Zoological Journal of the Linnean Society (2001), 132: 55–80. With 5 figures doi: 10.1006/zjls.2000.0263, available online at http://www.idealibrary.com on

A cladistic analysis of Siboglinidae Caullery, 1914 (Polychaeta, Annelida): formerly the phyla Pogonophora and Vestimentifera

GREG W. ROUSE

School of Biological Sciences A08, University of Sydney, NSW 2006, Australia

Received August 1999; accepted for publication June 2000

It has been proposed in recent years that the phyla Pogonophora and Vestimentifera are a derived clade of polychaete annelids. It has also been proposed that if this clade belongs among polychaetes, then the taxon name Pogonophora is misleading and should revert to a name first formulated for the group, Siboglinidae Caullery, 1914. This recommendation is adopted in this paper, and a cladistic study using terminals of ‘generic’ rank in the former Pogonophora (including Vestimentifera) is undertaken. The purpose of this is to assess which taxon names should now be used for clades within Siboglinidae, and to provide a revised taxonomy, based on phylogenetic principles. Another major aim is to assess the position of the vestimentiferan clade within Siboglinidae. The results show that Vestimentifera is the sister group to Sclerolinum, and this clade is then sister group to Frenulata, i.e. the remaining Siboglinidae. The results suggest that all taxa within Siboglinidae that are not genera or species are redundant, except for the following: Siboglinidae is defined as the first polychaete, and all its descendants, to have an gut occluded by expanded endoderm filled with chemoautotrophic bacteria, as seen in the holotype of Riftia pachyptila Jones, 1981. Monilifera can be defined based on apomorphy-based system such that it is the first siboglinid, and all its descendants, to have rings of chaetae (uncini) in the opisthosoma, as seen in the holotype of Sclerolinum magdalenae Southward, 1972. Vestimentifera can be defined as the first siboglinid and all its descendants to have a vestimentum as seen in the holotype of Riftia pachyptia. Frenulata is defined as the siboglinid, and all its descendants, to have a mid-trunk girdle, as seen in the holotype of Siboglinum weberi Caullery, 1914. The taxa of generic rank are not defined here since their monophyly was not investigated.  2001 The Linnean Society of London

ADDITIONAL KEYWORDS: phylogenetic taxonomy – systematics – phylogeny – Monilifera – Frenulata.

INTRODUCTION with reducing sediments, methane seeps, or with sunken terrestrial-plant debris. The varied and complex taxonomic history of Po- In his original description, Caullery (1914) noted gonophora and Vestimentifera represents one of the that Siboglinum weberi lacked an obvious digestive more fascinating tales in animal systematics. The fact tract, amongst other unusual features, and described that they tend to be found in deep-sea sediments it as having a dorsal nerve cord. He placed S. weberi resulted in the first member of this group, Siboglinum in a new family, Siboglinidae, but did not place it weberi Caullery, 1914, not being described until early within any other taxon, though he compared it with in the 20th century. There are now more than 100 deuterostomes such as hemichordates. Uschakov nominal species described, most from abyssal regions, (1933), apparently unaware of Caullery’s work, de- though exceptionally they are found in depths of less scribed a similar animal, Lamellisabella zachsi Us- than 100 m (Miura, Tsukahara & Hashimoto, 1997; chakov, 1933 from the north-eastern Pacific and placed Webb, 1964a). Some are large and spectacular mem- it in a new sabellid polychaete subfamily, Lamelli- bers of hydrothermal-vent communities (Jones, 1981a, sabellinae Uschakov, 1933. Johansson (1937, 1939) re- b), while others are smaller and found in association assessed the placement of L. zachsi, and decided it was not a polychaete. He erected a separate taxon name for it, Pogonophora, with the rank of class, but E-mail: [email protected] did not place it within any other taxon. Subsequent 55 0024–4066/01/050055+26 $35.00/0  2001 The Linnean Society of London 56 G. W. ROUSE workers (e.g. Beklemishev, 1944) then ranked Po- group, that of Siboglinidae Caullery, 1914. This name gonophora (with reference to Lamellisabella only) as change was also proposed by McHugh (1997) who, a phylum among deuterostomes. based on molecular sequence data on a variety of Ivanov (1951) compared Siboglinum and La- animals including a vestimentiferan, found that the mellisabella and was the first to recognize that both latter was nested among polychaetes. It has also been must belong to the same taxon and moved Siboglinum endorsed in two recent papers on the position of the weberi (and hence Siboglinidae) into Pogonophora. Iv- group (Halanych et al., 1998; Boore & Brown, 2000). anov (1952) described several new pogonophores and The suggestion by Rouse & Fauchald (1997) and later published a large monograph on the group (Iv- McHugh (1997) requires a reassessment of the utility anov, 1960, 1963). He regarded pogonophores as having of the current taxonomy of Pogonophora and Ves- deuterostome features such as radial cleavage, a dorsal timentifera, with both of these names treated, from nerve cord, and a tripartite coelom (formed by entero- this point on, as subsidiary to the name Siboglinidae. coely). Soon after, Webb (1964d) described the hitherto Here cladistic analyses are performed to assess which missing segmented, chaetal-bearing, posterior end taxon names should now be used for clades within (now called the opisthosoma). After this discovery some Siboglinidae. Another major aim is to assess the po- authors felt pogonophores were still deuterostomes sition of the vestimentiferan clade within Siboglinidae. (Ivanov, 1970, 1975a,b; Johansson, 1968), while others A new systematization, based on phylogenetic tax- suggested they were protostomes showing spiral cleav- onomy is then provided. age, a ventral nerve cord, chaetae and metameric segmentation (Liwanow & Porfirjewa, 1967; Nørre- BACKGROUND TO CURRENT SYSTEMATICS vang, 1970a,b; Southward, 1971b; George & South- Aspects of taxonomy within Siboglinidae (=Pogono- ward, 1973; van der Land & Nørrevang, 1975). phora and Vestimentifera) are briefly outlined here. The resolution of the placement of Pogonophora be- Further details are given in Table 1. Ivanov (1960, came more complicated with the description of La- 1963) divided the group referred to here as Frenulata mellibrachia barhami Webb, 1969a from slope depths (all Siboglinidae except for Sclerolinum and Ves- off California. Webb (1969a) placed L. barhami in a timentifera, see below) into Thecanephria and new pognophoran taxon, Vestimentifera. Later, closely Athecanephria. This was based on the development related taxa were found at hydrothermal vents, and of the anterior nephridial system. Unfortunately, it these massive worms were described by Jones (1981a, appears that the only taxa whose nephridia were in- b), who subsequently placed them in a separate vestigated by Ivanov were members of Siboglinum, phylum, Vestimentifera (Jones, 1985a). Jones (1985a) Oligobrachia (Ivanov, 1957) and Lamellisabella,and argued that, in spite of the many similarities between there is simply not enough information to assess the Vestimentifera and Pogonophora, Vestimentifera was utility of the nephridial system as a character. Never- more closely related to Annelida than to Pogonophora, theless, Ivanov (1960, 1963) used additional features thus justifying their separation. Southward (1988) con- such as spermatophore shape to justify his taxonomic sidered recognition of the phylum Vestimentifera as divisions. Within Athecanephria Ivanov (1960, 1963) untenable, and that vestimentiferans must belong in placed Oligobrachiidae Ivanov, 1957 with Birstenia the Pogonophora. This view was reinforced by Rouse Ivanov, 1952, Nereilinum Ivanov, 1961, Oligobrachia & Fauchald (1995) who listed eight synapomorphies Ivanov, 1957 (with Crassibrachia Southward, 1978a that grouped Pogonophora and Vestimentifera and and Unibrachium Southward, 1972 added later), and showed Jones’ (1985a) reasoning for erecting a phylum Siboglinidae with Siboglinum and Siboglinoides Iv- to be flawed. Molecular sequence data (Black et al., anov, 1961. Within Thecanephria he placed Poly- 1997; Kojima et al., 1997; Halanych, Lutz & Vrijenhoek, brachiidae Ivanov, 1952, with Cyclobrachia Ivanov, 1998) also suggest that Pogonophora and Ves- 1960, Diplobrachia Ivanov, 1960, Galathealinum Kir- timentifera form a monophyletic group. kegaard, 1956, Heptabrachia Ivanov, 1952, Poly- The idea postulated by Uschakov (1933) and Hart- brachia Ivanov, 1952, Sclerolinum Southward, 1961, man (1951, 1954) that Pogonophora are polychaetes and Zenkevitchiana Ivanov, 1957 [Choanophorus was revived by Bartolomaeus (1995), Nielsen (1995) Bubko, 1965 was added later, though this was then and Rouse & Fauchald (1995). Rouse & Fauchald questioned by (Webb, 1971)]; Lamellisabellidae with (1997) conducted a series of cladistic analyses of poly- Lamellisabella (and subsequently Siphonobrachia chaetes and showed that Pogonophora (including Ves- Nielsen, 1965), and Spirobrachiidae Ivanov, 1952 with timentifera) represents a member of a polychaete clade Spirobrachia Ivanov, 1952. This taxonomic system has called Sabellida. They argued that since the name remained largely unchanged, with the exception of the Pogonophora was misleading at this level, the name position of Sclerolinum (see below). of the group should revert to that of the first family When Webb (1969a) described the first ves- group name originally formulated for members of the timentiferan, Lamellibrachia barhami, he assigned CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 57

Table 1. Taxonomic arrangements of taxa considered in this paper from when they were considered as Pogonophora (including Vestimentifera). The taxa Frenulata and Monilifera are as formulated by Ivanov (1991). Athecanephria and Thecanephria are as formulated by Ivanov (1963) with some subsequent additional taxa. Vestimentifera is as formulated by Jones (1985a), with some subsequent additional taxa

Higher taxa Family rank Generic rank

Siboglinidae Siboglinum, Siboglinoides

Athecanephria Oligobranchiidae Oligobranchia, Nereilinum, Birstenia, Unibrachium, Crassibranchia∗

Frenulata Thecanephria Polybrachiidae Choanophorus, Cyclobrachia, Diplobrachia, Galathealinum, Heptabrachia, Polybrachia, Zenkevitchiana

Lamellisabellidae Lamellisabella, Siphonobrachia

Spirobrachiidae Spirobrachia

Monilifera Sclerolinidae∗∗ Sclerolinum∗∗

Escarpiidae Escarpia Lamellibrachiida Lamellibrachiidae Lamellibrachia

Basibranchia Ridgeiidae Ridgeia

Vestimentifera Tevniida Tevniidae Oasisia, Tevnia

Arcovestiidae∗∗∗ Arcovestia

? Alaysiidae Alaysia

Axonobranchia Riftiida Riftiidae Riftia

∗ Crassibrachia was originally placed in Polybrachiidae by Southward (1968) and then moved to Oligobrachiidae by Southward (1978a). ∗∗ Monilifera was erected by Ivanov (1991) to accommodate Sclerolinum, which he removed from Frenulata. ∗∗∗ Arcovestia was associated with Tevniida by Southward & Galkin (1997). this new taxon to a new class of Pogonophora, Af- containing the class Afrenulata, and Perviata con- renulata, new order, Vestimentifera, and new family, taining Frenulata. Subsequently, a separate phylum Lamellibrachiidae. He assigned all previously de- was erected for Obturata by Jones (1985a), which scribed pogonophore taxa to a new class Frenulata. The he called Vestimentifera because this was the most name Frenulata will be used through the remainder familiar name. The names Perviata and Obturata are of this paper to refer to all Siboglinidae, except for disregarded here, since they provide no additional Sclerolinum (see below) and Vestimentifera (Table 1), taxonomic information and Perviata (at the time) was since this represents the formulation found in some exactly the same taxonomic circumscription as the other recent papers (Ivanov, 1991; Ivanov & Se- older name Frenulata. Jones (1985a) divided Ves- livanova, 1992), though it should be noted that South- timentifera into Axonobranchia and Basibranchia on ward (1993, 1999) uses the name Perviata for this the structure of the branchial lamellae (i.e. palpal assemblage (and includes Sclerolinum). Jones (1981a) crown). In Axonobranchia he placed Riftiidae Jones, erected two subphyla within Pogonophora, Obturata 1981a with Riftia Jones, 1981a, and in Basibranchia; 58 G. W. ROUSE

Escarpiidae Jones, 1985a with Escarpia Jones, 1985a, species of the genus was used to determine the score. Lamellibrachiidae with Lamellibrachia; Ridgeiidae The five taxa with polymorphisms were Diplobrachia Jones, 1985a with Ridgeia; and Tevniidae Jones, 1985a (number of palps); Nereilinum (the presence of pinnules with Oasisia Jones, 1985a and Tevnia Jones, 1985a. and raised ventral glandular areas); Siboglinum (dir- Subsequently Alaysia spiralis Southward, 1991 placed ection of teeth in uncini); Siphonobrachia (direction in Alaysiidae Southward, 1991, and Arcovestia ivanovi of teeth in uncini); Unibrachium (zone of thickened Southward & Galkin, 1997 placed in Arcovestiidae papillae). Further explanation for each of these prob- Southward & Galkin, 1997 were erected. Both these lem areas can be found in Appendix 2. In future, the taxa were placed into Basibranchia. monophyly of each non-monotypic taxon does need to The taxon Sclerolinum was originally placed in Po- be assessed in more restricted analyses. No attempt lybrachiidae by Southward (1961). Subsequently was made here to identify apomorphies for the ter- Sclerolinum was placed into Sclerolinidae Webb 1964a, minals and some taxa are scored as exactly the same who regarded this taxon as the most plesiomorphic for all characters (i.e. Galathealinum, Heptabrachia, pogonophore. Ivanov (1991) and Ivanov & Selivanova and Polybrachia; Lamellisabella and Spirobrachia). (1992) noted similarities between Sclerolinum and Ves- timentifera on one hand, and Frenulata on the other OUTGROUP and so decided it should be placed into a new taxon, Monilifera, with equal rank to Frenulata and Ves- In five of the six cladistic analyses on polychaete re- timentifera (Table 1). lationships Rouse & Fauchald (1997) found Si- boglinidae (as Frenulata and Vestimentifera) to fall as the sister group to a clade comprised of Sabellariidae, MATERIAL AND METHODS Sabellidae, and Serpulidae. In the other analysis Si- boglinidae did appear as the sister group to tere- TERMINAL TAXA bellimorph polychaetes. These analyses differed on in The decision made here with regards to terminals was the number of taxa included, on the character coding to use taxa of the ‘generic’ rank and assume that they used and on a priori weighting of characters, On the are monophyletic. The type species of each genus was basis of the overall congruence of results found in not always used to score the characters since in many the various analyses in Rouse & Fauchald (1997), cases there was considerable missing information for Sabellariidae is chosen as the outgroup for this study, the types that could be supplemented by information though further study on the placement of Siboglinidae from other taxa in the genus. This means that the is admittedly required. Sabellariids have a pair of scoring for a terminal was in some cases based on peristomial palps, an anterior pair of large nephridia, information from a number of different nominal spe- and uncini (Rouse & Fauchald, 1997). This makes cies. Information from types was used where there them the most appropriate of the proximate taxa to was polymorphism for the terminal. Among ves- polarize the characters used here since tere- timentiferans this is not particularly problematic, since bellimorphs, sabellids and serpulids have prostomial six of the eight genera are monotypic anyway. Ridgeia palps, and terebellimorph polychaetes also lack the phaeophiale Jones, 1985a was recently made a syn- distinctive pair of large anterior nephridia (Rouse & onym of Ridgeia piscesae Jones, 1985a by Southward, Fauchald, 1997). Tunnicliffe & Black (1995), making this genus mono- typic, and Lamellibrachia, with five nominal species, and Escarpia with two nominal species presented no MORPHOLOGICAL FEATURES USED TO DEVELOP polymorphisms when it came to coding characters for CHARACTERS this study. Other monotypic siboglinid taxa include The morphology of Siboglinidae is reviewed here with Birstenia, Cyclobrachia, and Zenkevitchiana. Most special reference to those features that provided char- other Siboglinidae have a only a few nominal species, acters for the cladistic analysis. The characters are such as Crassibrachia (2), Diplobrachia (6), Ga- listed and justified Appendix 1 and 2 and the matrices lathealinum (3), Heptabrachia (7), Lamellisabella (7), provided in Appendix 3. Siboglinidae have unusual Oligobrachia (8), Nereilinum (2), Polybrachia (6), Scler- anatomy and there are several issues concerning their olinum (6), Siphonobrachia (2), and Unibrachium (2). basic structure that remain to be resolved, particularly This leaves Siboglinum as by far the largest taxon, over the position and delineation of the peristomium with 65 nominal species. In general, the taxa were and the first segment. A major factor contributing to anatomically relatively uniform, and presented little this is that the terminology used to describe them has difficulty in scoring for the characters used in this not been that used to described polychaete anatomy. study. There were, however, five instances where poly- Studies of larval development (see Bakke, 1990; South- morphisms were apparent within a terminal. In all of ward, 1988) now allow for a reinterpretation of their these cases the condition that is found in the type structure in terms of polychaete terminology. Note that CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 59 the interpretation offered here differs slightly from Siboglinum lack pinnules. The palps can be free from that of Rouse & Fauchald (1997). each other (e.g. Heptabrachia, Polybrachia), or fused together by the cuticle in frenulates such as Si- phonobrachia, Lamellisabella and Spirobrachia,and Prostomium and peristomium in all vestimentiferans. In two vestimentiferan taxa, The structure referred to as the protosoma by Ivanov Lamellibrachia and Alaysia, the outer palps fuse (1994), the tentaculomere by Webb (1969b), ‘segment 1’ (Jones, 1985a) to form lamellar sheaths (Fig. 1E). by Southward (1988), or the cephalic lobe by Southward Vestimentiferans have a paired structure called the (1993), would appear to be the prostomium and the obturaculum (Fig. 1E). Southward (1988) found that peristomium in most Siboglinidae (Fig. 1A–E). The the obturaculum develops after the larva has a number small conical prostomium (usually called the cephalic of palps, and that it had no counterpart with other lobe) is usually clearly distinguishable from the peri- siboglinids. In contrast Ivanov (1989) argued that the stomium but in adult vestimentiferans it is either obturaculum is in fact the first pair of palps to develop, absent, or completely surrounded by the palps (Fig. though they are quickly obscured by the other palps 1A–E). There are no eyes or other structures on the until a relatively late stage. Jones & Gardiner (1989) prostomium. The peristomium forms a complete ring, suggested that the first pair of palps (‘larval branchiae’) usually terminated by a clear groove (e.g. labelled s1 disappear, but did not ascertain the origin and de- fig. B92 in Ivanov, 1963) and bears the palps in most velopment of the obturaculum. Further investigation siboglinids, though, in vestimentiferans the de- seems required on the origin of the obturaculum. The limitation of the peristomium is uncertain and further adult obturaculum can have parasagittal (Oasisia, Rif- developmental studies are required (Fig. 1A–E). Note tia, Tevnia) or frontal musculature (Escarpia, La- that Rouse & Fauchald (1997) interpreted the region mellibrachia, Ridgeia). It can also be ornamented with bearing the frenulum or the vestimentum as being an axial rod (Escarpia, Oasisia, Riftia, Tevnia), and peristomial, but here it is considered to be segmental may have a terminal crust (Escarpia, Tevnia), or sau- (though further investigation is required; see below). A cers (Oasisia, Ridgeia). The obturacular stalk can be character based on whether the prostomium is clearly grooved (Alaysia, Arcovestia, Lamellibrachia, Oasisia, identifiable is used here. The uncertainty about the Ridgeia, Riftia, Tevnia)) or ridged (Escarpia, La- peristomium in vestimentiferans precludes the use of mellibrachia). The feature used to divide Ves- characters associated with this region at this time. timentifera into Axonobranchia and Basibranchia by Jones (1985a) is not informative in this analysis, since Palps only Riftia has the palps fused with the obturaculum The palps of Siboglinidae arise behind the larval pro- (Southward, 1991). totroch (Fig. 1B), and hence are peristomial structures (Rouse & Fauchald, 1997). There can be as few as a single palp (Siboglinum, Unibrachium),orapairof Segmented region palps (e.g. Crassibrachia, Diplobrachia, Nereilinum, A vexing question in siboglinid morphology is whether Sclerolinum). Those taxa with ‘numerous’ palps can the bulk of the body can be referred to as a single have from 8 or 9 (Cyclobrachia, Heptabrachia) to 14–40 segment or two segments (see Southward, 1971b). In (e.g. Lamellisabella, Polybrachia, Siphonobrachia, most siboglinids the region immediately behind the Zenkevitchiana), to hundreds (e.g. vestimentiferans, head, termed the mesosoma by Ivanov (1994), the Galathealinum, Spirobrachia). Sabellariidae (and frenulomere by Webb (1969b), and the forepart by many other polychaete taxa) have a pair of peristomial Southward (1993), bears a cuticular structure called palps (Rouse & Fauchald, 1997). Dividing the palpal the frenulum (Fig. 1A–D). In vestimentiferans the organization of Siboglinidae into homology hypotheses equivalent region is called the vestimental region (Fig. is difficult. The adult condition of having a pair of 1E) and has no frenulum (Gardiner & Jones, 1993). palps (Crassibrachia, Sclerolinum, Siboglinoides, etc.), The next body region is generally referred to as the or of having only a single palp (e.g. Siboglinum, Uni- trunk or metasoma (Ivanov, 1994; Southward, 1988). brachium) are seen here as clear primary homology Southward (1980, 1988) regarded the trunk plus the statements (Fig. 1B, C). Other taxa are regarded here area bearing the vestimentum, or frenulum, as a single as having ‘numerous’ palps (Fig. 1E). The palps of segment. However, Nørrevang (1970a) in describing most siboglinids have pinnules associated with them the early development of Siboglinum clearly described (Fig. 1C). The pinnules are comprised of a single cell the development of the diaphragm and it does suggest in most taxa (Ivanov, 1963), but in vestimentiferans that the forepart (or vestimental region) and trunk are the pinnules are multicellular (Selivanova, 1989). two (or more) segments, not one. This issue appears Members of Crassibrachia, Choanophorus, Nereilinum to require further investigation, and is not of major (one of two nominal species), Sclerolinum and some relevance here. 60 G. W. ROUSE

Figure 1. Features of Siboglinidae used to generate characters. A, generalized siboglinid. The prostomium and peristomium (bearing the palps) comprise what was formerly regarded as the protosoma. The next region (dark stipple) that has the frenulum, and terminates at the diaphragm, was formerly regarded as the mesosoma. This area may be part of the first segment. The trunk (light stipple) is either the bulk of the first segment or comprises the second segment. The trunk can have an anterior metameric papillate region dorsally, an area of thickened dorsal papillae and posterior rows or lines of dorsal papillae. There may also be posterior ventral raised glandular areas. The mid- region of the trunk has a girdle of uncini. The body terminates with the multi-segmented opisthosoma bearing peg- like chaetae or uncini (redrawn from Southward, 1975b). B, lateral view of a Siboglinum larva. The palp develops behind the ciliary band known as the prototroch, thus making it a peristomial structure. The limit of the peristomium is indicated based on comparison with adult morphology. The first segment may be the region that has the frenulum and terminates at the diaphragm, or this area may be only part of the first segment. The trunk then is either the bulk of the first segment or the second segment (redrawn from Southward, 1975b). C, lateral view of the anterior end of CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 61

The frenulum (or bridle) is a pair of cuticular crests Lamellibrachia and Escarpia are unusual in that there that run obliquely around the forepart (Fig. 1A–D). is a single mid-dorsal exit for the nephridia (Jones, Developmental evidence from Nereilinum suggests the 1988). A single pore for the pair of anterior nephridia frenulum develops from cuticular plaques (Ivanov, is found in sabellids and serpulid polychaetes, though 1994). Similar plaques are scattered on the vestimental in Sabellariidae there are separate openings for each region of vestimentiferans and just behind the palps of the two nephridia (Orrhage, 1980). Although Ivanov in Sclerolinum. The condition of scattered plaques in (1960, 1963) used nephridial structure as the basis for the vestimental region is scored as a state in the his taxonomy there is too little information across the character ‘Frenulum’ in the Multistate analysis, but a group to use his criterion as a character. frenulum proper is not considered present in Ves- The next body region, the trunk (possibly the second timentifera. However, in members of Sclerolinum there segment), comprises most of the body in siboglinids are two rows of plaques that positionally would appear (Fig. 1A). The anterior region (usually called the pre- justifiably to be called a frenulum (Ivanov, 1994). The annular region) often has two rows of papillae (Fig. vestimentum of vestimentiferans is a pair of lon- 1A, C). This ‘metameric’ region is absent in groups gitudinal flaps along the dorsal part of the vestimental such as Nereilinum and Sclerolinum which have lon- region that overlap mid-dorsally forming a longitudinal gitudinal ridges of pyriform glands. In ves- space over the segment (Fig. 1E). The vestimentum timentiferans there are scattered pyriform glands in also projects forward to form a collar around the base this area (Gardiner & Jones, 1993; Webb, 1969a). of the palpal crown. In most siboglinids the region Behind the anterior trunk section are more scattered bearing the frenulum terminates at the muscular dia- papillae followed, in some taxa (e.g. Oligobrachia, Hep- phragm with a clear external groove (Fig. 1A–C). In tabrachia), by a region of enlarged papillae and a Sclerolinum and vestimentiferans there is no clear ventral ciliated region (Fig. 1A, F). In some cases (e.g. demarcation (Fig. 1D, E). The pair of excretory organs Siboglinoides, Cyclobrachia) the papillae of this region are for the most part in the frenular or vestimental of the trunk in front of the uncini are simply scattered. region, and usually have separate openings on each A girdle of uncini in the mid-region of the trunk is side of the peristomium, or at the base of the ob- present in all siboglinids (Fig. 1A, B, H), except for turaculum in vestimentiferans. The vestimentiferans Sclerolinum and vestimentiferans. The uncini typically

Siboglinum pinnulatum Ivanov, 1960 showing the prostomium, peristomium with a single palp (bearing pinnules), and frenulum. Metameric papillae begin immediately behind the diaphragm (redrawn from Ivanov, 1963). D, lateral view of Sclerolinum sibogae showing a pair of palps and a frenulum. The prostomium is distinguishable as a projecting ventral lobe but the peristomium has yet to be demarcated. There is no clear diaphragm between the region bearing the frenulum and the trunk (redrawn from Southward, 1961). E, dorsal view of anterior end of Lamellibrachia satsuma, showing the obturaculum, ‘numerous’ palps that are fused into outer lamellar sheaths and the vestimentum. The vestimentum region is supposed to be homologous with the region bearing the frenulum in other siboglinids (redrawn from Miura et al., 1997). F, dorsal view of the region of thickened papillae of Polybrachia canadensis (Ivanov, 1962) (redrawn from Ivanov, 1963). G, dorsal view of girdle with two rows of uncini of Siboglinum caulleryi Ivanov, 1951 (redrawn from Ivanov, 1963). H, lateral view of girdle uncinus of Polybrachia annulata Ivanov, 1952 showing teeth facing in opposite directions (redrawn from Ivanov, 1963). I, peg-like chaeta from opisthosoma of Siboglinum poseidoni (drawn from micrographs in Flu¨ gel & Callsen-Cencic, 1992; Southward, 1993). J, dorsal view of Polybrachia canadensis showing girdle with two rows of uncini and posterior trunk papillae in rows (redrawn from Ivanov, 1963). K, lateral view of posterior trunk of Nereilinum murmanicum Ivanov, 1961, showing regularly spaced dorsal papillae and ventral glandular shields (redrawn from Ivanov, 1963). L, opisthosoma of Polybrachia canadensis showing a clear demarcation between the trunk and opisthosoma and the peg-like chaetae in each opisthosomal segment (redrawn from Southward, 1969). M, opisthosoma of Sclerolinum magdalenae Southward, 1972 showing rows of uncini in each segment. There is no clear separation between the trunk and the opisthosoma and the first row of uncini correspond to the girdle chaetae of most siboglinids (redrawn from Southward, 1972). N, opisthosoma of Arcovestia ivanovi showing rows of uncini on each segment (redrawn from Southward & Galkin, 1997). O, narrow spindle-like spermatophore of Siboglinum fedetovi Ivanov, 1957 with elongate filament (redrawn from Ivanov, 1963). P, broad, flattened leaf-like spermatophore of Lamellisabella johanssoni Ivanov, 1957, with elongate filament (redrawn from Ivanov, 1963). Q, rigid tube with funnels as found in Lamellisabella, Spirobrachia and vestimentiferans (redrawn from Webb, 1971). R, membranous and collapsed anterior end of tube as seen in many siboglinids (redrawn from Webb, 1971). Abbreviations: cb=ciliary band, d=diaphragm groove, f=frenulum, g=mid-trunk girdle of uncini, mp=metameric papillae, o=obturaculum, op= opisthosoma, outer sheath lamellae, p=prostomium, pa=palp, pe=peristomium, pi=pinnules, pg=peg-like chaetae, pp=line or row of posterior trunk papillae, pr=prototroch, ru=rows of uncini, s=septum, t=trunk, tp=thickened zone of papillae, tu=row of uncini on posterior trunk, v=vestimentum, vg=ventral glandular shields. 62 G. W. ROUSE lie as two pairs of semicircular bands on epidermal have been studied (e.g. Southward, 1982). According ridges (Fig. 1G). Behind the uncini there may be a to Southward (1982), this was previously referred to transverse row of dorsal papillae (e.g. Lamellisabella), as the medial coelomic cavity by Ivanov (1963). A or the papillae may be single at any one point and so transitory opening to the gut, either posteriorly or form a longitudinal row (e.g. Oligobrachia, Ner- anteriorly, has been shown in Siboglinum poseidoni eilinum). There may also be ventral glandular shields Flu¨ gel & Langhof 1983 by Callsen-Cencic & Flu¨ gel opposite the papillae (e.g. Siboglinum, Nereilinum) (1995) and in Ridgeia spp. (Jones & Gardiner, 1988; (Fig. 1A, J, K). In Sclerolinum and vestimentiferans Southward, 1988), and this appears to be the pathway there are only scattered papillae along the length of whereby bacteria are acquired to occupy the tro- the trunk. The trunk in most siboglinids terminates phosome. with an obvious septum and external groove (Fig. 1A, L). The remainder of the body is a short multi- Tubes segmented region called the opisthosoma, or telosoma (Fig. 1A, B, L–N). Southward (1972) and Ivanov (1994) The tubes of siboglinids are distinctive, and their struc- have noted that the opisthosoma of Sclerolinum and ture and variability was reviewed by Webb (1971), vestimentiferans (e.g. Ridgeia, Riftia) has no clear who also commented on their systematic value. Webb’s demarcation (Fig. 1M, N). It appears that chaetae in (1971) conclusion that there are two fundamental tube front of the first opisthosomal septum in these groups types in siboglinids is used here for character con- are at the end of the trunk, and so correspond to the struction (Fig. 1Q, R). He found that tubes could have a girdle of uncini on the trunk of other siboglinids. The collapsible anterior end (e.g. Oligobrachia, Nereilinum, anterior segments of the opisthosoma have chaetae Sclerolinum, Siboglinoides, Siboglinum), or it could be that, in Sclerolinum and vestimentiferans, are uncini rigid, often resembling a series of funnels stacked on in rows (Fig. 1M, N). In other siboglinids there are 4 each other (Choanophorus, Lamellibrachia, Spi- ‘peg-like’ chaetae in most segments (Fig. 1B, I, L). The robrachia, Lamellisabella). All vestimentiferans are uncini of nearly all siboglinids have two groups of teeth considered here to have these rigid tubes. Webb (1971) that face in opposite directions (Fig. 1H), a feature not found that some taxa that had been included in Poly- seen in polychaete uncini. It should be noted that brachia and Galathealinum by Ivanov (1963) probably Cyclobrachia auriculata Ivanov, 1960 and some mem- should be excluded from these taxa on the basis of bers of Diplobrachia, Siboglinum and Siphonobrachia their tube morphology, but did not resolve where they do have uncini where all teeth face in the same dir- should actually be transferred to. These nominal spe- ection (Ivanov, 1963; Nielsen, 1965). cies were not considered when coding their respective terminals for this study. Like many polychaetes, the tubes of Sclerolinum and Vestimentifera are attached Reproduction to hard substrates while other siboglinids are unique Males of all siboglinids, except Sclerolinum and ves- in having tubes that are buried in sediment for at least timentiferans, produce masses of broad, leaf-shaped a third of their length (Webb, 1971). or narrow, spindle-shaped spermatophores that are spawned into the water (Fig. 1O, P). Some taxa such MORPHOLOGICAL FEATURES NOT USED as Siphonobrachia and Zenkevitchiana have sper- matophores which seem to fall between the two states There are a number of features that have been used defined by Ivanov (1963). For Sclerolinum there were in siboglinid descriptions that are not implemented initial reports of spermatophores but these were later here. As mentioned above the organization of nephridia discounted. It would appear that in Sclerolinum and was used by Ivanov (1957) to erect Thecanephria and Vestimentifera sperm are spawned freely, or in un- Athecanephria. However, he only discussed de- enclosed bundles (spermatozeugmata) (Southward, scriptions for members of Siboglinum, Oligobrachia, 1971b; Southward & Coates, 1989), though the spawn- and Lamellisabella, and seems to have relied on other ing method is unknown for many in the latter taxon. features such as spermatophore structure to place taxa into Thecanephria or Athecanephria. Southward (1993) has added further data on Siphonobrachia and Gut showed that the distinctions between the Theca- Nutritional requirements for siboglinids are met nephria and Athecanephria conditions are not as clear through their symbiotic relationship with chemo- as Ivanov (1963) suggested. The lack of any published autotrophic bacteria that occupy cells (bacteriocytes) data for most of the taxa under investigation here in the expanded endoderm (trophosome). Adult si- precludes the use of any nephridial characters beyond boglinids have no obvious mouth and the gut lumen the one involving the number of excretory openings. is nearly completely occluded by the endoderm, though Most Siboglinidae would appear to have cuticular a small lumen does appear to be present in those that plaques on various regions of the body. Aspects of their CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 63 shape and distribution on papillae have been used using Sabellariidae as outgroup. Unknown character as a character to distinguish among nominal species states were coded with a ‘?’. Zero-length branches were (Ivanov, 1963). However, there has been no systematic collapsed and MULPARS was activated. Tree searches documentation of these structures across the group. It were performed using the random addition search appears that, at the hierarchical level used here, no command with 100 replicates. Analysis of character purpose would be served by including this data owing optimizations were performed using PAUP and Mac- to difficulties in establishing primary homology hy- Clade 3.07 (Maddison & Maddison, 1997). Where there potheses and polymorphisms. This problem is dis- are various possible most-parsimonious trans- cussed by Nielsen (1965). The papillae that are found formations for a given character the ACCTRAN trans- behind the girdle of chaetae in many siboglinids are formation is used here, where possible, since this characterized as being in repeated rows in many taxa maintains the primary homology hypotheses to a large and as a series of individual papillae forming a line in extent (de Pinna, 1991). For Multistate characters others (Oligobrachia, Nereilinum, Siboglinoides, Si- there is often no way that one can choose between boglinum). However, as discussed by Nielsen (1965) alternative optimizations and they are all discussed. there is considerable polymorphism of these features The matrices are shown in Appendix 3 and can also and so a general character based on the presence of be found, along with the resulting tree files from the orderly rows, or a line, of papillae was used. following addresses: TreeBASE (http://herb- aria.harvard.edu/treebase/), and the author’s website (http://www.bio.usyd.edu.au/papers/gregr/) CLADISTIC ANALYSIS Problems with character coding for cladistic analyses have been addressed by several authors (e.g. Pleijel, RESULTS 1995; Wilkinson, 1995b). Here the same strategy used by Rouse & Fauchald (1997) is implemented in that The three separate ways of treating the data gave both Absent/Present coding (Pleijel, 1995) and Mul- results that had the same overall implications in terms tistate coding is used. For the Absent/Present matrix of the revised taxonomy adopted here, but there were all 44 characters were treated either as of equal weight some minor differences that will be outlined. The A/ (as the A/Pe analysis) even if they were linked (e.g. Pe analysis resulted in 240 most parsimonious trees characters based on the substructures of the ob- of length 79 (consistency index CI=0.56; retention turaculum are linked to the presence of the ob- index RI=0.86; rescaled consistency index RC=0.48). turaculum in the first place). Weighting to control for The strict consensus tree is shown in Figure 2A. The such linkage was applied, as in Rouse & Fauchald A/Pw analysis resulted in 1104 shortest trees of length (1997), for the characters with linkage (as the A/Pw 66.75 (CI=0.55; RI=0.86; RC=0.48). These 1104 trees analysis). This meant that all arguably independent are not congruent with the shortest trees from the A/ characters were given a weight of 1. Subsidiary char- Pe analysis and represent, when reweighted according acters were given a weight of 0.5. These characters the A/Pe system, 684 trees that correspond to trees of were those involving substructures of the multiple length 80, and 420 trees that are of length 81, i.e. one palps (‘lamellar sheaths’ ‘fused palps’), obturaculum or two steps longer than the A/Pe analysis results. The (‘frontal’ or ‘parasagittal’ obturacular musculature, ‘ax- strict consensus tree of the A/Pw trees is shown in ial rod’, ‘grooved’ or ‘ridged’ obturacular stalk) pinnules Figure 2B. The Multistate analysis found 6112 most (‘single-celled’ or ‘multicellular’), and the types of sper- parsimonious trees of length 58 steps (CI=0.70; RI= matophores (‘leaf’ or ‘spindle’). Two characters (‘crust’ 0.89; RC=0.63). When the length of these trees is and ‘saucers’) that were subordinate to the presence measured using the A/Pe matrix they range between of an axial rod in the obturaculum were given a weight 79 and 86 steps, with the 112 trees of length 79 of 0.25. For the Multistate analysis, coding various representing a subset of the 240 shortest trees found features that are arguably ‘homologous’ as states in the A/Pe analysis. The strict consensus of the Mul- within one character (e.g. spermatophores can be tistate shortest trees is very similar to that of the A/ ‘broad’ or ‘narrow’) was used. For taxa where such Pe analysis and is shown in Figure 2C. characters are inapplicable, a ‘–’ is used that is treated In the all three analyses there were several con- as a missing state by the program, with various in- sistent clades: herent problems (Nixon & Davis, 1991; Platnick, Gris- wold & Coddington, 1991; Pleijel, 1995; Wilkinson, 1. Vestimentiferans (in the traditional usage, Table 1995a). 1) formed a clade that was the sister group to Cladistic analyses were performed using PAUP∗ ver- Sclerolinum and this clade is the sister group to sion 4.0b4a (Swofford, 2000). Trees were rooted, and the remaining ingroup taxa. hence characters polarized (Nixon & Carpenter, 1993), 2. The remaining siboglinids, (Frenulata in Table 1), 64 G. W. ROUSE

Figure 2. Consensus trees from the three parsimony analyses. In all three analyses Sclerolinum was always the sister group to the vestimentiferan clade. The relationships among the other siboglinids (Frenulata) varied in each analysis and none of them matched the currently accepted groupings of the genera. A, strict consensus of 240 shortest trees (length 79) generated from the A/Pe matrix. B, strict consensus trees of 1104 shortest trees (length 66.75) found using the A/Pw matrix. C, strict consensus trees of 6112 shortest trees (length 58) found with the Multistate matrix. CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 65

formed a clade, and of these Nereilinum and Crassi- lost in vestimentiferans and some other siboglinids). brachia always formed a grade with respect to the The clade formed by Sclerolinum and vestimentiferans remaining taxa. was supported by the presence of uncini at the posterior 3. Cyclobrachia, Lamellisabella, Siphonobrachia and end of the trunk (26), scattered trunk papillae (28), Spirobrachia formed a clade. uncini only in all posterior segments (33), rings of chaetae in posterior segments (36) and, under an In A/P coding, under both weighting schemes, La- ACCTRAN transformation that assigned sperm- mellibrachia and Escarpia form a clade in all trees that atozeugmata to Sclerolinum, the presence of sperm- was the sister group to the remaining vestimentiferans. atozeugmata (40). The monophyly of Frenulata was Within this clade the relationships varied among the indicated by the presence of a number of features: a trees, but Ridgeia and Oasisia were always sister clear diaphragm groove at the beginning of the trunk groups, and formed a clade with Tevnia (Fig. 2A, B). (21), a mid-trunk girdle of uncini (25), a zone of In the A/Pw analysis there was considerable topological thickened papillae on the trunk (27) (subsequently variation in relationships within Frenulata, which was lost in some taxa), ventral glandular shields on the largely caused by the variable placement of Di- posterior trunk (29) (subsequently lost and regained plobrachia. However, Zenkevitchiana was always the in one clade), dorsal papillae in a line or rows on the sister group to the clade formed by Cyclobrachia, La- posterior trunk (30), a marked opisthosomal dia- mellisabella, Siphonobrachia and Spirobrachia (Fig. phragm (31), ‘peg’-like chaetae (35), spermatophores 2B). (37), that are narrow (39) (subsequently lost in one In Multistate coding there was considerable vari- clade), and a tube that lies buried unattached in the ability in the topologies for the relationships among sediment (44). vestimentiferans (Fig. 2C). However, the relationships The monophyly of the vestimentiferan clade was among Frenulata in the Multistate analysis were ba- indicated by the gain of an indistinct prostomium (1), sically the same as found by the A/Pe analysis in that: ‘numerous’ palps (4), pinnules (5), that are multi-celled (1) Choanophorus was always the sister group to the (7), a cuticle that fuses the palps (at least in part) (8), remaining Frenulata. an obturaculum (10), a vestimentum (18), and the (2) Diplobrachia, Galathealinum, Heptabrachia and presence of a rigid tube (42). It was also supported by Polybrachia always formed a clade. the loss of a pair of palps (3) and loss of a frenulum (19) (3) This clade was always sister group to the Cy- (under ACCTRAN). The clade formed by Cyclobrachia, clobrachia, Lamellisabella, Siphonobrachia and Lamellisabella, Siphonobrachia and Spirobrachia was Spirobrachia clade. supported in all A/P analyses trees by the (homoplastic) (4) Zenkevitchiana and Siboglinoides always formed presence of fused palps (8). The sister group of this a grade with respect to the clade described in 3. clade (in the A/Pe analysis), comprised of Diplobrachia, Galathealinum, Heptabrachia and Polybrachia was TRANSFORMATIONS supported by the (homoplastic) presence of a zone of thickened papillae (27), and the loss of scattered pa- The tree used to show transformations for the A/P and pillae (28). The sister group relationship of these two Multistate matrices is one of the 240 shortest trees clades was supported by the loss of narrow sper- (length=79) found in the A/Pe analysis that is also matophores (39), and the presence of broad spermato- one of the 6112 trees found in the Multistate analysis. phores (38). With the exception of vestimentiferans, The results of the A/Pw analysis are the same as the all taxa with ‘numerous’ palps (4) formed a clade but A/Pe and Multistate analyses with respect to the major this (and the loss of a pair of palps, 3) was the only clades. The transformations that supported the major feature supporting its monophyly. The other re- clades in all trees in each of the three analyses are lationships shown in Figure 3 were also only generally outlined here (Figs 3, 4) and summarized in Table 2. supported by one or a few character transformations. The situation was similar in the Multistate analysis A/P analyses and the transformations for the same tree as for the In both A/P analyses the monophyly of Siboglinidae A/Pe analysis is shown in Figure 4. was supported by the presence of a frenulum (19) (under ACCTRAN, and this means this feature was lost in vestimentiferans), a trunk (22), an opisthosoma Multistate analyses (32), uncini with groups of teeth facing in opposite Most of the transformations occur in the basal part directions (34) (subsequently lost in Cyclobrachia and of the Multistate analysis trees and there was little Siphonobrachia), a gut lumen that is largely occluded support for clades at more restrictive levels (Fig. 4). (41), and a tube with a collapsible anterior end (43) When there are multiple equally parsimonious trans- (under ACCTRAN, and this means this feature was formations for a character, the nature of unordered 66 G. W. ROUSE

Table 2. List of unambiguous apomorphies (i.e. those that occur in each most parsimonious transformation) found in both the A/P and Multistate coding analyses supporting the four major clades named in this study. ∗ACCTRAN transformation (see text for details)

A/P analyses Multistate analysis Unambiguous apomorphies Unambiguous apomorphies

Siboglinidae Presence of: Frenulum∗ (19); Trunk (22); Presence of: Frenulum (12:1); Trunk (15:1); (=Pogonophora) Opisthosoma (32); Uncini opposed teeth (34); Ridges with pyriform glands on the anterior Occluded gut (41); Collapsible tube∗ (43) trunk (16:1); Opisthosoma (21:1); Uncini with opposed teeth (25:1); Occluded gut (28:1); Collapsible tube (29:1) Monilifera Presence of: Uncini at posterior of trunk (26); Presence of: Rings of opisthosomal chaetae (24:1); Scattered trunk papillae (28); Uncini only in all Spermatozeugmata∗ (26:2). Also various posterior segments (33); Rings of opisthosomal ambiguous transformations. chaetae (36); Spermatozeugmata∗ (40) Frenulata Presence of: Anterior Diaphragm (21); Mid- Presence of: Anterior diaphragm (14:1); Ventral trunk with chaetal girdle (25); Zone of thick glandular shields (19:1); Buried tube (30:1). Also papillae (27); Ventral glandular shields (29); various ambiguous transformations. Dorsal papillae (lines or rows) (30); Opisthosomal diaphragm (31); ‘Peg’ chaetae (35); Spermatophores (37); that are Narrow (39); Buried tube (44) Vestimentifera Presence of: Indistinct prostomium (1); Presence of: Indistinct prostomium (1:1); ’Numerous’ palps (4); Pinnules (5), that are ‘Numerous’ palps (2:2); Multicelled pinnules (3: multicelled (7); Fused palps (8); Obturaculum 1); Fused palps (4:1); Obturaculum (6:1); (10); Vestimentum (18); Rigid tube (42). Loss of: Vestimentum (11:1); Frenulum area has Paired palps (2); Frenulum∗ (19) scattered plaques only (12:2); Anterior trunk with metameric papillae (16:3); Rigid tube (29:2).

multistate characters means it can be impossible to on the branch where the node above (or terminal) decide along which branch transformations between unambiguously has that state. Most of these am- states for that particular character may occur. For biguous transformations occur in the basal part of the example, Multistate character 17 (Segment 1 or 2 tree. This means that there a number of trans- (Trunk) with girdle of uncini) has three states: 0. formations that support the monophyly of Siboglinidae Absent, 1. Present middle, 1. Present posteriorly. Al- that are not shown, or that various apomorphies for lowing for further outgroup considerations, in all trees the two major subclades of Siboglinidae are not shown. there is a transformation to either state 1 or 2 below The unambiguous transformations for Siboglinidae the ingroup node (i.e. Siboglinidae) or states 1 and 2 were the presence of the following features: a frenulum evolved independently from the absent state. We can (12, state 1), a trunk (15, state 1), ridges with pyriform discount the latter possibility on the basis that the glands on the anterior trunk (16, state 1), an op- two conditions of the girdle should be accepted as isthosoma (21, state 1), uncini with teeth facing the homologous in line with principles outlined by de Pinna opposite direction (25, state 1), an occluded gut (28, (1991), and so should not be seen to have evolved state 1), a collapsible tube (29, state 1). The un- independently. But there is no justifiable way to choose ambiguous transformations for the Sclerolinum plus between the hypothesis that the girdle of uncini was vestimentiferan clade were the presence of rings of initially (i.e. plesiomorphic for Siboglinidae) in the chaetae in the posterior segments (24, state 1), and mid-trunk (state 1) and then transformed to the pos- the presence of spermatozeugmata (26, state 2) (under terior trunk (state 2) along the branch leading to the an ACCTRAN transformation that assigned sperm- node joining Sclerolinum with vestimentiferans, or atozeugmata to Sclerolinum). There were a number of vice-versa. The approach taken here is therefore to other ambiguous transformations that could serve as indicate on Figure 4 that a transformation either has synapomorphies for this clade, namely the presence of taken place below the node from which the branch a scattered papillae in the anterior trunk (17, state 2), originated, or will occur along that branch. This is a girdle of uncini at the posterior end of the trunk (18, indicated by placing the character state in brackets state 2), scattered papillae on the posterior trunk (20, CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 67

Figure 3. Character transformation on one of the 240 shortest trees from that A/Pe analysis that also matched one of the shortest trees from the Multistate character analysis. Slashes on branches indicate transformation of the character below the node. Character details are in the text, and listed in Appendix 1. Character numbers in plain text indicate a transformation from absent to present and that there is no homoplasy for that character. Underlined characters show homoplasy in the form of convergence and outlined characters represent reversals to the absent state. Characters with the letters ACC after them means that the ACCTRAN transformation requires the state change along that branch, but that other possible transformations (i.e. for less inclusive clades) are equally parsimonious. The clades Siboglinidae, Monilifera (=Vestimentifera plus Sclerolinum) and Frenulata are all supported by a number of synapomorphies. 68 G. W. ROUSE

Figure 4. Character transformations on one of the shortest trees from that Multistate analysis that is the same as one of the trees resulting from the A/Pe analysis. Slashes on branches indicate transformation of the character below the node ‘above’. Character details are in the text and listed in Appendix 1. Arrows after a character number indicate a transformation to the state listed. Brackets around a character state indicate that it must have transformed to that state below the next node but may also have transformed to this state below a preceding node. Character states in plain text indicate there is no homoplasy for that state. Underlined characters show homoplasy in the form of convergence, and outlined characters represent reversals to the absent state. The ∗ next to a transformation for character 26 (Sperm packaging) under ACCTRAN assigns Sclerolinum with spermatozeugmata (though it has yet to be observed), thus making it a synapomorphy grouping it with vestimentiferans. All taxa with no spermatophores were assigned with ? for character 27 (Spermatophore type) and these were all assigned state 0 (Narrow, spindle- shaped). I have indicated the transformation to this state 27→0 where it is actually logical to do so, along the branch that supports the clade Frenulata. The clades Siboglinidae, Monilifera, and Frenulata (all defined as taxa in the Discussion) are each supported by a number of synapomorphies. CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 69 state 2), no clear separation between the trunk and opisthosoma (22, state 0), and that all chaetae in posterior segments are uncini (23, state 1). The monophyly of Frenulata was unambiguously supported by the presence of a clearly grooved dia- phragm at the beginning of the trunk (14, state 1), the presence of ventral glandular shields in the posterior trunk (19, state 1), and the presence of a tube that lies freely in the sediment (30, state 1). The ambiguous transformations that could serve as synapomorphies for this clade were the presence of a zone of thickened papillae (17, state 1), the presence of a girdle of uncini in the mid-trunk (18, state 1), the presence of a line or rows of papillae on the posterior trunk (20, state 1), a clear separation between the trunk and op- isthosoma (22, state 1), that all chaetae in posterior segments are ‘peg-like’ (23, state 2), and the presence of spermatophores (26, state 1). The character based on spermatophore shape (27) can only logically be applied to those taxa with spermatophores i.e. Fre- nulata. However, given the topology of the shortest trees, and since taxa without spermatophores were scored with ‘–’ for this character, all optimizations applied give these taxa the state 0 (‘Spindle-shaped spermatophores’). In fact, the only place that the state 0 should be applied is below the node for Frenulata. While there is a most parsimonious transformation for spermatophores to be plesiomorphic for Siboglinidae as a whole, it is not appropriate for a possible trans- formation to the presence of spindle-shaped sper- matophores below this node. To do this would mean that the vestimentiferan plus Sclerolinum clade would, inappropriately, have to be considered as having this state. The only other clade that is consistently sup- ported by more than one synapomorphy is Ves- timentifera, where there are nine (Fig. 4; Table 2).

DISCUSSION

There have been two previous explicit hypotheses of Figure 5. Previous hypotheses about the evolution of the phylogeny of Siboglinidae, and these are shown in Siboglinidae. A, tree outlining ideas of Ivanov (1963). Figure 5. Both of these hypotheses were developed Taxa such as Choanophorus, Nereilinum, Siboglinoides, before the description of a number of taxa, including all Siphonobrachia and vestimentiferans were unknown, or vestimentiferans (Ivanov, 1963; Webb, 1964b). Ivanov not considered, when this tree was published. Ivanov (1963) argued that the plesiomorphic siboglinid had (1963, 1970) argued that the hypothetical ancestor had six palps, and that this had been elaborated into a six palps and that this condition had been maintained in complex array of palps in groups such as Spirobrachia, members of Heptabrachia and Oligobrachia (he depicted reduced to pair of palps (for Diplobrachia), or to a this by drawing a thicker line to these terminals from the hypothetical ancestor) with other taxa showing reductions single palp as in Siboglinum. Ivanov (1963) suggested or elaborations from this number. B, tree outlining ideas that Heptabrachia and Oligobrachia retained many of Webb (1964b). Taxa such as Choanophorus, Si- plesiomorphic siboglinid features, and depicted this by phonobrachia and vestimentiferans were unknown when drawing a thicker line to these terminals from the this tree was published. Webb (1964b) argued that the hypothetical ancestor (Fig. 5A). Webb (1964b) in- hypothetical ancestor had two palps and that Sclerolinum corporated information about Sclerolinum, which had closely resembled this hypothetical ancestor. not been included in Ivanov’s discussion, and argued that the plesiomorphic condition for Siboglinidae was 70 G. W. ROUSE to have a pair of palps. Webb suggested that Sclero- group to the rest of Siboglinidae, the lengths were 39 linum represented the most plesiomorphic group of for the A/Pe matrix, 34 for the A/Pw matrix and 22 for Siboglinidae (Fig. 5B), but in other respects (allowing the Multistate matrix (Table 3). Wilcoxon signed rank for other added taxa) his phylogenetic hypothesis was tests showed that these constrained topologies based similar to that of Ivanov (1963). Ivanov (1970) re- on Webb (1964b) were significantly longer than the iterated his support for his earlier, (Ivanov, 1963), unconstrained trees (Table 3). hypothesis and rejected Webb’s (1964b) suggestion re- While both the hypotheses expressed in Figure 5 garding Sclerolinum as plesiomorphic. can be disregarded as not being parsimonious ex- The results shown here do not lend support to the planations of the available data, the overall congruence hypotheses of Webb (1964b) or Ivanov (1963, 1970). in the results found here (Figs 2–4) suggests some However, the differences in the taxa that were avail- new conclusions may be drawn. The plesiomorphic able for consideration between then and now do have condition for palps found in all analyses was for there to be taken into account. Allowing for the fact that to be a single pair, in agreement with Webb (1964b). vestimentiferans were unknown when Webb (1964b) From the paired condition, the ‘numerous’ palp con- developed his hypothesis, excluding them from the dition appears to have developed twice, once for Ves- results obtained here places Sclerolinum as sister timentifera and once for a large unnamed clade in group to the remaining Siboglinidae. However, the Frenulata (Figs 4, 5). Within this frenulate clade there remaining details of his proposed phylogeny largely have been subsequent reductions to two palps again followed Ivanov’s (1963). If the other taxa that were (Diplobrachia) or to a single palp (Siboglinum and not included in either Webb’s or Ivanov’s proposed Unibrachium). Other plesiomorphic conditions for si- phylogenies are also excluded from the topologies pro- boglinids that subsequently transform would appear posed here, then the results still show that their hy- to be: potheses are not parsimonious explanations of the (1) The frenulum, which has become scattered plaques data. To demonstrate this further I performed analyses on the vestimentum of vestimentiferans. In- with the A/P and Multistate matrices on the taxa only terestingly, Sclerolinum major Southward, (1972) included in Ivanov’s (1963) tree. Characters that were has only scattered plaques instead of a frenulum. uninformative for this restricted taxon set were ex- (2) The tube with a collapsible anterior end has cluded (i.e. characters 1–3, 5–7, 9–26, 30–37, 40, 41, changed into a more rigid one with funnels in 44, or Multistate characters 1–3, 5–16, 18, 20–26, 28, vestimentiferans, Choanophorus and the clade 30). This resulted in 13 shortest trees of length 12 for comprised of Lamellisabella, Siphonobrachia,and the A/Pe trees, 8 shortest trees of length 9.5 for the A/ Spirobrachia. Pw trees and 12 shortest trees of length 6 for the Multistate matrix. These results all provided trees There have been two explicit phylogenetic hy- that were congruent, given the deleted taxa, with the potheses proposed for Vestimentifera. Jones (1988) results of the complete taxa analyses performed here. illustrated his Linnaean taxonomy of the group in a In contrast, when applying Ivanov’s (1963) topology to dendrogram format (shown in Table 1). The results of the data matrices, the lengths were 20 for the A/Pe the present A/P analyses do not support his hypothesis matrix, 16.5 for the A/Pw matrix, and 11 for the in that Riftia (Axonobranchia) is nested within the Multistate matrix. Wilcoxon signed rank tests (Temple- Basibranchia. Also the proposed sister group re- ton, 1983) showed that two of the three constrained lationship between Tevnia and Oasisia was not re- topologies were significantly longer than the un- covered. However, the clades comprised of constrained trees (Table 3). The exception was the (Lamellibrachia, Escarpia) and (Oasisia, Tevnia, Multistate data set assessing Ivanov’s (1963) hypo- Ridgeia) proposed by Jones (1988) were found in the thesis, and this may be due to the very small data set. A/P analyses. When the same method was applied to Webb’s (1964b) Black et al. (1997) and Halanych et al. (1998) found taxon set (also with uninformative characters excluded that vestimentiferans that live at ‘cold-seeps’ (Es- i.e. A/P characters 1, 2, 7, 9–22, 25, 26, 30–37, 40, 41, carpia, Lamellibrachia) formed a grade with respect 44 or Multistate characters 1, 5–15, 18, 20–26, 28, 30), to the remaining vestimentiferans, all of which are then this resulted in 5 shortest trees of length 25 for associated with hydrothermal vents. It should be noted the A/Pe matrix, 202 shortest trees of length 22.5 for that neither of these two studies, based on molecular the A/Pw trees, and 2 shortest trees of length 14 for sequences, included data for Alaysia or Arcovestia, the Multistate trees. As for the restricted analyses both of which are associated with hydrothermal vents based on Ivanov’s (1963) hypothesis, these topologies (Southward, 1991; Southward & Galkin, 1997). In were also congruent with the complete analyses pre- contrast to the analyses based on molecular data, the sented here. In contrast, when applying Webb’s (1964b) results from the A/P analyses here both show that the topology, and Sclerolinum is assumed to be the sister cold-seep taxa form a clade that is the sister group CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 71

Table 3. Comparison of tree lengths using the taxa shown in Ivanov’s (1963) and Webb’s (1964b) respective phylogenetic hypotheses (Fig. 5). Analyses were either: (1) constrained to their topologies (Fig. 5), or (2) unconstrained parsimony analyses. Only the taxa shown by Webb or Ivanov were used, and characters that were uninformative for these restricted taxon sets were excluded from the A/P or Multistate matrix (see text). Wilcoxon signed rank tests (Templeton, 1983) showed that constrained topologies were significantly longer than the unconstrained trees in 5 out of the 6 analyses. The exception was the Multistate data set assessing Ivanov’s (1963) hypothesis and this may be due to the very small data set

Ivanov, 1963 Webb, 1964b (Fig. 5A) (Fig. 5B)

A/Pe unconstrained 12 steps 25 steps A/Pe constrained 20 steps 39 steps P<0.0384∗ P<0.0039∗ A/Pw unconstrained 9.5 steps 22.5 steps A/Pw constrained 16.5 steps 34 steps P<0.0384∗ P<0.0261∗ Multistate unconstrained 6 steps 14 steps Multistate constrained 11 steps 22 steps P<0.1025 P<0.0231∗

to the hydrothermal-vent taxa. Black et al. (1997) Vestimentiferaclade, there is currently 13 family group proposed that the hydrothermal-vent associated fauna taxa, and the current rules of nomenclature would evolved from vestimentiferan ancestors associated then enforce 12 of these to be synonymized with the with cold seeps. While the topology of vestimentiferan oldest available name, Siboglinidae. There are also relationships found here differs from that of Black et additional nomenclatural problems in that well-de- al. (1997), consideration of the habitats occupied by fined names such as Vestimentifera have now been other members of Siboglinidae would suggest that their shown to represent subgroups within Siboglinidae. hypothesis is correct. The lack of resolution found in An alternative to the Linnaean system is to apply the the Multistate analysis suggests that further detailed names within the framework of phylogenetic taxonomy study of vestimentiferans is required, particularly on (e.g. de Queiroz & Gauthier, 1992). The name Si- Alaysia and Arcovestia. boglinidae can be retained and given a phylogenetic definition, instead of a Linnaean one (see below). Fur- thermore, the abandonment of all traditional supra- SYSTEMATICS generic names within Siboglinidae, except for The first issue that requires comment is the formal Vestimentifera, Monilifera, and Frenulata is re- name for the group under study. As outlined in the commended (the relationships within the less inclusive Introduction, Rouse & Fauchald (1997) and McHugh groupings are not analysed here, and will require (1997) suggested that Pogonophora plus Vesti- separate studies and revisions). The usefulness in mentifera, having been inferred to have a sister group selecting the names Vestimentifera, Monilifera, and among polychaete annelids, should revert to the name Frenulata for the major subgroups of Siboglinidae lies Siboglinidae. Rouse & Fauchald (1997) justified their in that their circumscription (see Fig. 2) is largely recommendation by stating that the name Pogon- consistent with recent, traditional taxonomy (e.g. ophora may become misleading when applied as a Ivanov, 1991). The previously 12 ‘sunk’ family names subgroup name within polychaetes. By changing the will, in the absence of Linnaean ranks, not have to be name to the first name erected for the group, Si- synonymized; they will instead simply be considered as boglinidae, a ‘fresh’ start is made in terms of the currently unused names for parts within Siboglinidae. taxonomic status of the group. This suggestion has They may be activated later following further study been endorsed in several recent papers (Halanych et al., and better resolution. Here a conservative approach 1998; Boore & Brown, 2000), and is adopted throughout is taken and only four well-supported taxon names are this paper. However, within the Pogonophora– defined. 72 G. W. ROUSE

Based on the results here from all three forms of Multistate analyses there is so much topological vari- analysis I define Siboglinidae as the first polychaete, ation among vestimentiferans that no further sub- and all its descendants, to have an occluded gut (with division of the group can be made. I recommend the endoderm presumably occupied by chemo- abandoning Axonobranchia and Basibranchia as taxon autotrophic bacteria) as seen in the holotype of Riftia names. I also recommend that the vestimentiferan pachyptila Jones, 1981a. Only one of the several apo- names of family rank also be abandoned. Firstly, under morphies that support this clade (others include a the current Linnaean system of nomenclature, these frenulum, trunk, opisthosoma, uncini with opposing names are all junior synonyms of Siboglinidae. Also, teeth, and collapsible tube, see Figs 3, 4) is used to with the exception of Tevniidae containing Oasisia and define the taxon name. If all of the apomorphies were Tevnia, they are all monotypic, and hence ‘empty’ taxa. used to define Siboglinidae, then essentially the last Tevniidae was also shown to be paraphyletic in the A/ of these features to evolve would actually identify the P analyses. common ancestor linked to the name Siboglinidae. The taxon Frenulata, as formulated by Ivanov New taxa may be described that do not have all these (1991), was found in all analyses here, and I re- features and so would be excluded from the taxon. The commend that the name Frenulata continue to be choice of which apomorphy to use is hence arbitrary, applied as a clade name within Siboglinidae. This but I suggest that the presence of an occluded gut may grouping represents all Siboglinidae, with the ex- be a key feature in the evolution of this group and is ception of Sclerolinum and vestimentiferans. The an appropriate feature to use for the definition of the monophyly of this clade was supported by numerous name. synapomorphies, and as a taxon Frenulata can be In all analyses, the same two major clades were defined as the first siboglinid, and all its descendants, found within Siboglinidae. In one, Sclerolinum was to have a mid-trunk girdle, as seen in the holotype of placed as the sister group to vestimentiferans. Thus, Siboglinum weberi (see Southward, 1961). The pres- Vestimentifera represents a derived clade of Si- ence of a frenulum, which was used by Webb (1969a) to boglinidae, and its exclusion from this group, as pro- name the taxon Frenulata is actually a plesiomorphic posed by Jones (1985a,b), cannot be sustained. This feature for Siboglinidae. result was foreshadowed by Southward (1993: 332) Within Frenulata the taxon Athecanephria, erected who noted that several features of Sclerolinum ‘‘suggest by Ivanov was not supported in this analysis. Rather a link with the Obturata (Vestimentifera)’’. Ivanov Athecanephria taxa (see Table 1) consistently formed (1991) had also noted similarities between Sclerolinum a grade, a result actually implied by Webb’s (1964b) and vestimentiferans and removed the former from representation of the group’s phylogeny (Fig. 5B). If Frenulata. However, rather than group Sclerolinum with vestimentiferans, he placed it into a new taxon, Choanophorus is not considered, Thecanephria did Monilifera, with equal rank to Frenulata and Ves- form a clade in all A/Pe and Multistate analyses, but timentifera. I suggest, rather than make a new name, this was only supported by the loss of ventral glandular that the name Monilifera now be applied to the Sclero- shields. In the A/Pw analysis the variable placement linum plus Vestimentifera clade. The taxon name Mon- of Diplobrachia means that Thecanephria was not ilifera can be defined based on apomorphy-based consistently supported as monophyletic. Thecanephria system such that it is the first siboglinid, and all its and Athecanephria were erected based on the structure descendants, to have rings of chaetae (uncini) in the of the anterior nephridia by Ivanov (1957), but there opisthosoma, as seen in the holotype of Sclerolinum has never been a comprehensive survey to assess magdalenae Southward, 1972. A number of other apo- whether this is a useful systematic feature. Instead of morphies from the A/P analyses could also be used to nephridial organization, the shape of spermatophores aid in define this taxon but these ended as being has usually been used as a guide for the placement of ambiguous transformations in the Multistate analysis taxa into either Athecanephria (with narrow ‘spindle- (see Fig. 4). Within Monilifera, the taxon name Ves- shaped’ spermathecae) and Thecanephria (with broad timentifera can be defined as the first siboglinid and ‘leaf-shaped’ spermathecae). However in the present all its descendant to have a vestimentum as seen in study, the presence of ‘leaf-shaped’ spermathecae did the holotype of Riftia pachyptia. not serve as a synapomorphy for Thecanephria, since As discussed above, the results indicate that Jones’s Zenkevitchiana has narrow spermathecae (Figs 3, 4). division of Vestimentifera into Axonobranchia and Ba- This means that ‘leaf-shaped’ spermatophores evolved sibranchia has little utility. Firstly, Ridgeia is the only from a ‘spindle-shaped’ condition within Thecanephria. member of Axonobranchia and so Axonobranchia is Since Athecanephria is consistently paraphyletic, and an ‘empty’ taxon. Also, since in the A/P analyses, the monophyly of Thecanephria is not indicated, I Axonobranchia is always nested among the other ves- recommend abandoning these taxon names. timentiferans, Basibranchia is paraphyletic. In the The family level taxa used by Ivanov (1963) that CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 73 contain more than one genus; Lamellisabellidae, Oli- the manuscript and to two anonymous reviewers for gobrachiidae, Polybrachiidae, and Siboglinidae (see their interesting comments. This study was supported Table 1), were consistently found to be paraphyletic or by an Australian Research Council QEII Research polyphyletic in this study. Since the recommendation Fellowship. that the name Siboglinidae be adopted for the ingroup taxa in this analysis has been followed here, all taxa of family rank are to be considered synonyms of Si- REFERENCES boglinidae anyway. However, the fact that none of the Adegoke OS. 1967. Pogonophora from the northeastern names of family rank, either in Frenulata or Ves- Pacific: First records from the Gulf of Tehuantepec, Mexico. timentifera, was found to be monophyletic lends sup- Pacific Science 21: 188–192. port to their elimination as formal names. The Bakke T. 1990. Pogonophora. In: Adiyodi KG, Adiyodi RG, exceptions are, of course, those families that contain eds. Reproductive biology of invertebrates. Volume IV, Part a single genus and hence are essentially ‘empty’ taxa B Fertilization, development, and parental care. Chichester: with no utility. Given the fact that there was a lack of John Wiley and Sons, 37–48. resolution and some difference between the analyses Bartolomaeus T. 1995. Structure and formation of the in terms of the relationships within Frenulata, I sug- uncini in Pectinaria koreni, Pectinaria auricoma (Tere- gest that no other taxa within this clade be named at bellida) and Spirorbis spirorbis (Sabellida): implications this time. Further study is required on the taxa at for annelid phylogeny and the position of the Pogonophora. generic rank, since several may well be paraphyletic Zoomorphology 115: 161–177. assemblages. Beklemishev VN. 1944. Osnovy sravintel’noi anatomii be- spozvonochnykh. [Principles of the Comparative Anatomy CONCLUSIONS of Invertebrates.]. Moscow: Akademia Nauk. Black MB, Halanych KM, Maas PAY, Hoeh WR, Hashi- The results shown here show a number of mor- moto J, Desbruyeres D, Lutz RA, Vrijenhoek RC. phological features that support the monophyly of Si- 1997. Molecular systematics of vestimentiferan tubeworms boglinidae. They also show clear placement of the from hydrothermal vents and cold-water seeps. Marine vestimentiferan clade as the sister group to Sclero- Biology 130: 141–149. linum within Siboglinidae. Boore JL, Brown WM. 2000. Mitochondrial genomes of While the name Pogonophora is eliminated here Galathealinum, and Platynereis: Sequence and gene ar- as a taxon name, there is no reason why the name rangement comparisons indicate that Pogonophora is not ‘pogonophores’ or ‘beard worms’ cannot be used as a phylum and Annelida and Arthropoda are not sister taxa. informal name, much the same way as ‘ragworms’ and Molecular Biology & Evolution 17: 87–106. ‘fanworms’ are used for the polychaete taxa Nereididae Bubko OV. 1965. A new representative of the Pogonophora and Sabellidae respectively. The taxon names Fre- – Choanophorus indicus gen. n., sp. n. Zoologiska Zhurnal nulata, Monilifera and Vestimentifera are retained and 44: 1670–1677. are defined according to principles of phylogenetic Callsen-Cencic P, Flu¨ gel HJ. 1995. Larval development taxonomy. They are all contained within the taxon and the formation of the gut of Siboglinum poseidoni Flu¨ gel Siboglinidae. All other names, with the exception of and Langhof (Pogonophora, Perviata). Evidence of pro- those with the rank of genus or species, are considered tostomian affinity. Sarsia 80: 73–89. here to be redundant because they are ’empty’ taxa, Caullery M. 1914. Sur les Siboglinidae, type nouveau d’in- or represent paraphyletic or polyphyletic assemblages. verte´bre´s receuillis par l’expe´dition du Siboga. Comptes rendus de l’Academie des sciences, Serie III 158: 2014–2017. de Pinna MCC. 1991. Concepts and tests of homology in NOTE ADDED IN PROOF the cladistic paradigm. Cladistics 7: 367–394. de Queiroz K, Gauthier J. 1992. Phylogenetic taxonomy. A new paper (Halanych, Feldman & Vrijenhoek, 2001) Annual Review in Ecology and Systematics 23: 449–480. based on molecular evidence using 18S rDNA and 16S Flu¨ gel HJ. 1990. A new species of Siboglinum Pogonophora rDNA has shown that Sclerolinum brattstromi is closer from the North Atlantic and notes on Nereilinum mur- to Vestimentifera than to other Siboglinidae. This manicum Ivanov. Sarsia 75: 233–241. result corroborates the findings shown in this paper Flu¨ gel HJ, Callsen-Cencic P. 1992. New observations on based on morphology. the biology of Siboglinum poseidoni Flu¨ gel & Langhof (Pogonophora) from the Skagerrak. Sarsia 77: 287–290. ACKNOWLEDGEMENTS Flu¨ gel HJ, Callsen-Cencic P. 1993. A new species of the genus Siboglinum (Pogonophora) from the North Atlantic Thanks to D. J. Patterson (University of Sydney) for off Portugal. Sarsia 78: 255–264. facilities and advice. Also thanks to A. Simpson (Uni- Flu¨ gel HJ, Langhof I. 1983. A new hermaphroditic po- versity of Sydney) and Fredrik Pleijel (Muse´um Na- gonophore from the Skagerrak. Sarsia 68: 131–138. tional d’Histoire Naturelle) for comments on a draft of Gardiner SL, Jones ML. 1993. Vestimentifera. In: Harrison 74 G. W. ROUSE

FW, Rice ME eds. Microscopic anatomy of invertebrates, Ivanov AV. 1994. On the systematic position of Ves- volume 12: Onychophora, Chilopoda and lesser Pro- timentifera. Zoologische Jahrbu¨ cher Abteilung fu¨ r tostomata. New York: Wiley-Liss, 371–460. Systematik, Geographie, und Biologie der Tiere 121: 409– George JD, Southward EC. 1973. A comparative study 456. of the setae of Pogonophora and polychaetous Annelida. Ivanov AV, Selivanova RV. 1992. A new pogonophoran Journal of the Marine Biological Association of the United living on rotten wood, Sclerolinum javanicum sp. Biologiya Kingdom 53: 397–401. Morya 1992: 27–33. Gupta BL, Little C. 1969. Studies on Pogonophora. II. Johansson KE. 1937. U¨ ber Lamellisabella zachsi und ihre Ultrastructure of the tentacular crown of Siphonobrachia. systematische Stellung. Zoologischer Anzeiger 117: 23–26. Journal of the Marine Biological Association of the United Johansson KE. 1939. Lamellisabella zachsi Uschakow, ein Kingdom 49: 717–741. Vertreter eine neuen Tierklasse Pogonophora. Zoologiska Halanych KM, Lutz RA, Vrijenhoek RC. 1998. Evolu- Bidrag fra˚n Uppsala 18: 253–268. tionary origins and age of vestimentiferan tube-worms. Johansson KE. 1968. Pogonophora. In: Helmcke JG, Starck Cahiers de Biologie Marine 39: 355–358. D, Wermuth H, eds. Handbuch der Zoologie, gegru¨ ndet on Halanych KM, Feldman RA, Vrijenhoek RC. 2001. Mo- Willy Ku¨ kenthal 3(2) Lief. 18. 1–50. lecular evidence that Sclerolinum brattstromi is closely Jones ML. 1981a. Riftia pachyptila, new genus, new species, related to vestimentiferans, not frenulate pogonophorans) the vestimentiferan worm from the Gala´pagos Rift geo- Siboglinidae, Annelida). Biological Bulletin (in press.) thermal vents (Pogonophora). Proceedings of the Biological Hartman O. 1951. Fabricinae (Featherduster Polychaetous Society of Washington 93: 1295–1313. annelids) in the Pacific. Pacific Science 5: 379–391. Jones ML. 1981b. Riftia pachyptila Jones: Observations on Hartman O. 1954. Pogonophora Johansson, 1938. Sys- the vestimentiferan worm from the Gala´pagos Rift. Science tematic Zoology 3: 183–185. 213: 333–336. Ivanov AV. 1951. On including the genus Siboglinum Caul- Jones ML. 1985a. On the Vestimentifera, new phylum: Six lery in the class Pogonophora. (In Russian, English sum- new species, and other taxa, from hydrothermal vents and mary). Doklady Akadami Nauk SSSR 76: 739–742. elsewhere. Bulletin of the Biological Society of Washington Ivanov AV. 1952. New Pogonophora from the Far Eastern 6: 117–158. Seas. Zoologicheskii Zhurnal 28: 372–391 (in Russian). Jones ML. 1985b. Vestimentiferan pogonophores: their bio- Ivanov AV.1957. Neue Pogonophora aus dem nordwestlichen logy and affinities. In: Morris SC, George JD, Gibson R, Platt HM, eds. The origins and relationships of lower Teil des Stillen Ozeans. Zoologische Jahrbu¨ cher Abteilung invertebrates. The Systematics Association Special Vol. 28. fu¨ r Systematik, Geographie, und Biologie der Tiere 85: Oxford: Clarendon Press, 326–342. 431–500. Jones ML. 1988. The Vestimentifera, their biology, sys- Ivanov AV. 1960. Pogonophores. Fauna S.S.S.R. N.S. 75. tematic and evolutionary patterns. Oceanologica Acta, Spe- Moscow: Academiia Nauk S.S.S.R (in Russian). cial Volume 8: 69–82. Ivanov AV. 1961. Deux genres nouveaux de Pogonophores Jones ML, Gardiner SL. 1985. Light and scanning electron diplobrachiaux Nereilinum et Siboglinoı¨des. Cahiers de microscopic studies of spermatogenesis in the vesti- biologie marine 2: 381–387. mentiferan tube worm Riftia pachyptila (Pogonophora: Ob- Ivanov AV. 1962. New pognophores from the eastern part turata). Transactions of the American Microscopical Society of the Pacific Ocean. II. Heptabrachia ctenophora sp. n. 104: 1–18. and H. canadensis sp. n. (In Russian). Zoologiska Zhurnal Jones ML, Gardiner SL. 1988. Evidence for a transient 41: 893–900. digestive tract in Vestimentifera. Proceedings of the Bio- Ivanov AV. 1963. Pogonophora. London: Academic Press. logical Society of Washington 101: 423–433. Ivanov AV. 1970. Verwandtschaft und Evolution der Po- Jones ML, Gardiner SL. 1989. On the early development gonophoren. Zeitschrift fu¨ r Zoologische Systematik und of the vestimentiferan tube worm Ridgea sp. and ob- Evolutionsforschung 8: 109–119. servations on the nervous system and trophosome of Ridgea Ivanov AV. 1971. New Pogonophora from the Atlantic and sp. and Riftia pachyptila. Biological Bulletin. Marine Bio- Pacific Oceans. Journal of Zoology 164: 271–304. logical Laboratory, Woods Hole, Mass 177: 254–276. Ivanov AV. 1975a. Embryonalentwicklung der Pogonophora Kirkegaard JB. 1956. Pogonophora, Galathealinum bruuni, und ihre systematische Stellung. Zeitschrift fu¨ r Zoologische n. gen. n. sp., a new representative of the class. Galathea Systematik und Evolutionsforschung Sonderheft 1: 10–44. Report 2: 79–83. Ivanov AV. 1975b. Observations of embryonic development Kojima S, Segawa R, Hashimoto J, Ohta S. 1997. Mo- in Pogonophora. 2. Taxonomic status of Pogonophora. (In lecular phylogeny of vestimentiferans collected around Russian, English summary). Zoologicheskii zhurnal 54: Japan, revealed by the nucleotide sequences of mito- 1125–1154. chondrial DNA. Marine Biology 127: 507–513. Ivanov AV. 1989. Morphological nature of obturacles in Liwanow NA, Porfirjewa NA. 1967. Die Organisation der Pogonophora. (In Russian, English summary). Doklady Pogonophoren und deren Beziehungen zu den Polycha¨ten. Akademii nauk SSSR 308: 758. Biologische Zentralblatt 86: 177–204. Ivanov AV. 1991. Monilifera – A new subclass of Po- Maddison WP, Maddison DR. 1997. MacClade Version gonophora. Doklady Akademii Nauk, USSR 319: 505–507. 3.07. Sunderland; Sinauer Associates. CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 75

McHugh D. 1997. Molecular evidence that echiurans and Southward EC. 1975b. Pogonophora. In: Giese AC, Pearse pogonophorans are derived annelids. Proceedings of the JS, eds. Reproduction of Marine Invertebrates. California: National Academy of Sciences of the United States of Amer- Academic Press, 124–156. ica 94: 8006–8009. Southward EC. 1978a. Description of a new species of Miura T, Tsukahara J, Hashimoto J. 1997. La- Oligobrachia (Pogonophora) from the North Atlantic, with mellibranchia satsuma, a new species of vestimentiferan a survey of the Oligobrachiidae. Journal of the Marine worms (Annelida: Pogonophora) from a shallow hydro- Biological Association of the United Kingdom 58: 357–366. thermal vent in Kagoshima Bay, Japan. Proceedings of the Southward EC. 1978b. A new species of Lamellisabella Biological Society of Washington 110: 447–456. from the north Atlantic. Journal of the Marine Biological Nielsen C. 1965. Four new species of Pogonophora from the Association of the United Kingdom 58: 713–718. Atlantic Ocean off southern Florida. Bulletin of Marine Southward EC. 1980. Regionation and metamerisation in Science 15: 964–986. Pogonophora. Zoologische Jahrbu¨ cher (Anatomie und On- Nielsen C. 1995. Animal evolution. Oxford: Oxford Uni- togenie der Tiere) 10: 264–275. versity Press. Southward EC. 1982. Bacterial symbionts in Pogonophora. Nixon KC, Carpenter JM. 1993. On outgroups. Cladistics Journal of the Marine Biological Association of the United 9: 413–426. Kingdom 62: 889–906. Nixon KC, Davis JI. 1991. Polymorphic taxa, missing values Southward EC. 1988. Development of the gut and seg- and cladistic analysis. Cladistics 7: 233–241. mentation of newly settled stages of Ridgeia (Ves- Nørrevang A. 1970a. On the embryology of Siboglinum timentifera): implications for relationship between and its implications for the systematic position of the Vestimentifera and Pogonophora. Journal of the Marine Pogonophora. Sarsia 42: 7–16. Biological Association of the United Kingdom 68: 465–487. Nørrevang A. 1970b. The position of Pogonophora in the Southward EC. 1991. Three new species of Pogonophora, phylogenetic system. Zeitschrift fu¨ r Zoologische Systematik including two vestimentiferans, from hydrothermal sites und Evolutionsforschung 8: 161–172. in the Lau Back-arc Basin (Southwest Pacific Ocean). Orrhage L. 1980. On the structure and homologues of the Journal of Natural History 25: 859–881. anterior end of the polychaete families Sabellidae and Southward EC. 1993. Pogonophora. In: Harrison FW, Rice Serpulidae. Zoomorphologie 96: 113–168. ME, eds. Microscopic anatomy of invertebrates, vol. 12 Platnick NI, Griswold CE, Coddington JA. 1991. On Onychophora, Chilopoda and lesser Protostomata. New missing entries in cladistic analysis. Cladistics 7: 337–343. York: Wiley-Liss, 327–369. Pleijel F. 1995. On character coding for phylogeny re- Southward EC. 1999. Development of Perviata and Ves- construction. Cladistics 11: 309–315. timentifera (Pogonophora). Hydrobiologia 402: 185–202. Rouse GW, Fauchald K. 1995. The articulation of annelids. Southward EC, Brattegard T. 1968. Pogonophora of the Zoologica Scripta 24: 269–301. northwest Atlantic: North Carolina region. Bulletin of Rouse GW, Fauchald K. 1997. Cladistics and polychaetes. Marine Science 18: 836–875. Zoologica Scripta 26: 139–204. Southward EC, Coates KA. 1989. Sperm masses and sperm Selivanova RV. 1989. Homology of branchial filaments in transfer in a Vestimentiferan, Ridgeia piscesae Jones 1985 Vestimentifera to palpi in Pogonophora. Doklady Akademii (Pogonophora Obturata). Canadian Journal of Zoology 67: nauk SSSR 308: 760–761. 2776–2781. Southward EC. 1961. Pogonophora. Siboga Expedition 25: Southward EC, Galkin SV. 1997. A new vestimentiferan 1–22. (Pogonophora, Obturata) from hydrothermal vent fields Southward EC. 1968. On a new genus of pogonophore from in the Manus back-arc basin (Bismarck sea, Papua New the western Atlantic Ocean, with descriptions of two new Guinea, southwest Pacific Ocean). Journal of Natural His- species. Bulletin of Marine Science 18: 182–190. tory 31: 43–55. Southward EC. 1969. Growth of a pogonophore: a study of Southward EC, Tunnicliffe V, Black M. 1995. Revision of Polybrachia canadensis with a discussion of the de- the species of Ridgeia from northeast Pacific hydrothermal velopment of taxonomic characters. Journal of Zoology 157: vents, with a redescription of Ridgeia piscesae Jones (Po- 449–467. gonophora, Obturata equals Vestimentifera). Canadian Southward EC. 1971a. Pogonophora of the northwest At- Journal of Zoology 73: 282–295. lantic: Nova Scotia to Florida. Smithsonian Contributions Swofford DL. 2000. PAUP∗. Phylogenetic Analysis Using to Zoology 88: 1–29. Parsimony (∗and Other Methods). Version 4. Sunderland, Southward EC. 1971b. Recent researches on the Po- Massachusetts: Sinauer Associates. gonophora. Oceanography and Marine Biology, An Annual Templeton AR. 1983. Phylogenetic inference from re- Review 9: 193–220. striction endonuclease cleavage site maps with particular Southward EC. 1972. On some Pogonophora from the Carib- reference to the evolution of humans and the apes. Evolu- bean and the Gulf of Mexico. Bulletin of Marine Science tion 37: 221–244. 22: 739–776. Uschakov PV. 1933. Eine neue Form aus der Familie Southward EC. 1975a. New Pogonophora from Indonesia. Sabellidae (Polychaeta). Zoologischer Anzeiger 104: 205– Records of the Australian Museum 29: 441–451. 208. 76 G. W. ROUSE van der Land J, Nørrevang A. 1975. The systematic po- (24) Anterior of segment 1 (or 2) trunk with ridges and sition of Lamellibrachia (Annelida, Vestimentifera). Zeit- pyriform glands. schrift fu¨ r Zoologische Systematik und Evolutionsforschung (25) Mid-part of segment 1 (or 2) (Trunk) with uncinal Sonderheft 1: 86–101. girdle. (26) Segment 1 (or 2) (Trunk) with uncinal girdle pos- Webb M. 1964a. Additional notes on Sclerolinum brattstromi teriorly. (Pogonophora) and the establishment of a new family, (27) Segment 1 (or 2) (Trunk) with zone of thickened Sclerolinidae. Sarsia 16: 47–58. papillae. Webb M. 1964b. Evolutionary paths within the phylum (28) Segment 1 (or 2) (Trunk) with scattered papillae. Pogonophora. Sarsia 16: 59–64. (29) Posterior of segment 1 (or 2) (trunk) with raised Webb M. 1964c. A new bitentaculate pogonophoran from ventral glandular shields. Hardangerfjorden, Norway. Sarsia 15: 49–55. (30) Posterior of segment 1 (or 2) (trunk) with papillae Webb M. 1964d. The posterior extremity of Siboglinum dorsal papillae in rows or a line. fiordicum (Pogonophora). Sarsia 15: 33–36. (31) Marked opisthosomal diaphragm. Webb M. 1969a. Lamellibrachia barhami, gen. nov. sp. nov. (32) Opisthosoma. (33) Posterior segments with uncini only. (Pogonophora), from the northeast Pacific. Bulletin of (34) Uncini with teeth in two groups facing opposite Marine Science 19: 18–47. directions. Webb M. 1969b. Regionation and terminology of the po- (35) Posterior chaetae ‘peg-like’. gonophoran body. Sarsia 38: 9–24. (36) Posterior chaetae form rings. Webb M. 1971. The morphology and formation of the po- (37) Spermatophores. gonophoran tube and its value in systematics. Zeitschrift (38) Spermatophores broad (leaf-like). fu¨ r Zoologische Systematik und Evolutionsforschung 9: (39) Spermatophore narrow (spindle-like). 169–181. (40) Spermatozeugmata. Wilkinson M. 1995a. Arbitrary resolutions, missing entries, (41) Gut occluded. and the problem of zero-length branches in parsimony (42) Tube rigid with funnels. (43) Tube membranous and collapses anteriorly. analysis. Systematic Biology 44: 108–111. (44) Tube buried in sediment. Wilkinson M. 1995b. A comparison of two methods of char- acter construction. Cladistics 11: 297–308.

(B) Multistate characters APPENDIX 1 Some characters are binary and then there are mul- tistate characters subsidiary to these in some sense. CHARACTERS USED FOR THE A/P AND MULTISTATE Scoring for taxa for the less general characters when ANALYSES they were scored as absent (0) for the more general (A) Absent/Present characters characters is a ‘–’. Taxa where the condition for a char- acter was unknown were scored with ‘?’. All characters are binary with 0 for Absent and 1 for Present. Taxa where the condition for a character was (1) Prostomium indiscernible: (0) Absent, (1) Present unknown were scored with ‘?’. (2) Adult palps: (0) Pair of palps, (1) Single palp, (2) (1) Prostomium indiscernible. ‘Numerous’ palps (2) Adult with single palp. (3) Palpal pinnules: (0) Absent, (1) Present (multi- (3) Adult with a pair of palps. celled), (2) Present (single-celled) (4) Adult with ‘numerous’ palps. (4) Palps fused: (0) Absent, (1) Present (5) Pinnules on palps. (5) Outer sheath lamellae: (0) Absent, (1) Present (6) Palp pinnules single-celled. (6) Obturaculum: (0) Absent, (1) Present (7) Palp pinnules multi-celled. (7) Obturaculum musculature: (0) Parasagittal, (1) (8) ‘Numerous’ palps fused via cuticle. Frontal (9) Some palps form outer sheath lamellae. (8) Obturaculum with axial rod: (0) Absent, (1) Present (10) Obturaculum. (9) Obturaculum axial rod with: (0) Saucers, (1) Crust (11) Obturacular musculature parasagittal. (10) Obturaculum stalk: (0) Grooved, (1) Ridged (12) Obturacular musculature frontal. (11) Vestimentum: (0) Absent, (1) Present (13) Obturaculum with an axial rod. (12) Frenulum: (0) Absent, (1) Present, (2) Scattered (14) Obturaculum with terminal saucers. plaques only (15) Obturaculum with terminal crust. (13) Single exit for pair of anterior nephridia: (0) Absent, (16) Obturaculum stalk grooved. (1) Present (17) Obturaculum stalk ridged. (14) Diaphragm with clear external groove: (0) Absent, (18) Vestimentum. (1) Present (19) Frenulum. (15) Segment 1 (or 2) forms elongate trunk: (0) Absent, (20) Single exit for anterior pair of nephridia. (1) Present (21) Clear diaphragm groove at beginning of trunk. (16) Anterior segment 1 (or 2) (Trunk) with glands: (0) (22) Segment 1 (or 2) forms elongate trunk. Smooth, (1) Ridges, (2) Metameric papillae (23) Anterior of segment 1 (or 2) trunk with metameric (17) Papillae in anterior segment 1 (or 2) (Trunk) : (0) papillae. Absent, (1) Thickened zone, (1) Scattered CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 77

(18) Segment 1 (or 2) (Trunk) with uncinal girdle: (0) Scoring largely based on Webb (1969a), van der Land & Absent, (1) Present middle, (1) Present posteriorly Nørrevang (1975). An opisthosoma has been found in (19) Ventral glandular shields: (0) Absent, (1) Present Lamellibrachia columna and L. satsuma (Miura et al., (20) Posterior of segment 1 (or 2) (trunk) with papillae: 1997; Southward, 1991). (0) Absent, (1) Line or Rows, (2) Scattered Oasisia Jones, 1985a (21) Opisthosoma: (0) Absent, (1) Present Oasisia alvinae Jones, 1985a; only nominal species. (22) Opisthosomal diaphragm: (0) Absent, (1) Present Scoring based on Jones (1985a) and Southward & Galkin (23) Posterior segment chaetae: (0) Uncini and others, (1997). Nothing is known about sperm packaging. (1) All uncini, (2) ‘Peg-like’ chaetae Ridgeia Jones, 1985a (24) Posterior chaetae: (0) Notopodial and neuropodial, Ridgeia piscesae Jones, 1985a; only nominal species (1) Form rings after Southward et al. (1995) synonymized R. phae- (25) Uncini with teeth: (0) Facing same direction, (1) ophiale Jones, 1985a with R. piscesae. Two groups facing opposite directions. Scoring based on Jones (1985a), Southward & Coates (26) Sperm packaging: (0) Absent, (1) Spermatophore, (1989), and Southward & Galkin (1997). (2) Spermatozeugmata Riftia Jones, 1981a (27) Spermatophore shape: (0) Narrow (spindle), (1) Riftia pachyptila Jones, 1981a; only nominal species. Broad (leaf) Scoring based on Jones (1985a), Jones & Gardiner (1985) (28) Gut occluded: (0) Absent, (1) Present and Southward & Galkin (1997). (29) Tube: (0) Mixture of organic and inorganic, (1) Tevnia Jones, 1985a Organic and anterior collapses, (2) Organic with Tevnia jerichonana Jones, 1985a; only nominal species. rigid opening Scoring based on Jones (1985a) and Southward & Galkin (30) Tube lies in sediment: (0) Absent, (1) Present (1997). Nothing is known about sperm packaging.

MONILIFERA APPENDIX 2 Sclerolinum Southward, 1961 NOTES ON TERMINALS AND SCORING OF Sclerolinum sibogae Southward, 1961; five further nom- SIBOGLINIDAE inal species (see Ivanov & Selivanova, 1992; Southward, Terminal taxa are listed in alphabetical order under the 1972). more inclusive taxa adopted here; Monilifera containing Scoring based on Southward (1972), Ivanov & Se- Sclerolinum plus Vestimentifera, and Frenulata con- livanova (1992), and Webb (1964a; 1964c). Members of taining all other Siboglinidae. The type species of the Sclerolinum all have a pair of elongate palps that are genera are listed, along with information about how easily broken (Webb, 1964a). A frenulum is present as a many other taxa are currently included in the taxon. row of cuticular plates in some taxa, though Sclerolinum All references that were used in scoring are cited and major Southward, 1972 has only scattered plaques, as details are given about scoring where there was am- in vestimentiferans. It is assumed here that a frenulum biguity in the descriptions or polymorphism within the is the plesiomorphic condition for Sclerolinum. There is taxon, in which case data from the type species was no clear diaphragm identifying the beginning of the used. trunk according to (Webb, 1964a), but Southward (1980) noted an oblique band of muscle that seemed to be the MONILIFERA diaphragm, though there is no external sign of this. VESTIMENTIFERA Ivanov (1994) argued that the region bearing the frenulum is extremely long in Sclerolinum and that a Alaysia Southward, 1991 diaphragm is present. In this study the criterion adopted Alaysia spiralis Southward, 1991; only nominal species. is based on a clear external marking identifying the Scoring based on Southward (1991) and Southward & diaphragm, and Sclerolinum does not have this. Further Galkin (1997). There is no information about the pres- investigation is, however, required. Southward (1968) ence of pinnules on the palps, the musculature of the suggested the anterior part of the trunk has two lines obturaculum, nephridia, or sperm packaging. of pyriform glands. Southward (1972) showed that there Arcovestia Southward & Galkin, 1997 are uncini at the very end of the trunk, immediately in Arcovestia ivanovi Southward & Galkin, 1997; only nom- front of the first opisthosomal segment. Southward inal species. (1961) originally described spermatophores in Scler- Scoring based on Southward & Galkin (1997). There is olinum sibogae, but Southward (1971b) notes there is no information about the presence of pinnules on the no spermatophore. Whether the sperm are packaged as palps, the musculature of the obturaculum, nephridia, spermatozeugmata is not known. For the Multistate or sperm packaging. matrix this meant that Sclerolinum was scored as having Escarpia Jones 1985a either free spawning or spermatozeugmata. Escarpia spicata Jones 1985a and Escarpia laminata Jones 1985a. FRENULATA Scoring based on (Jones, 1985a) and Southward & Gal- kin, (1997). There is no information about the posterior Birstenia Ivanov, 1952 end of the body, or sperm packaging. Birstenia vitjasi Ivanov, 1952; only nominal species. Lamellibrachia Webb, 1969a Scoring based on Ivanov (1963). The posterior end is Lamellibrachia barhami Webb, 1969a and four other unknown. nominal species (see Miura et al., 1997). Choanophorus Bubko, 1965 78 G. W. ROUSE

Choanophorus indicus Bubko, 1965; only nominal spe- Scoring based on Ivanov (1963) and Southward (1978a). cies. Polybrachia Ivanov, 1952 Scoring based on Bubko (1965) and Southward (1969). Polybrachia annulata Ivanov, 1952; three nominal spe- The spermatophores are described as ‘band-shaped’ by cies in Ivanov 1963), including Krampolineum galathae Bubko (1965) and this is treated here as being the Kirkegaard, 1956. Southward & Brattegard (1968) de- narrow condition. scribed two other members and Southward (1969) trans- Crassibrachia Southward, 1968 ferred Heptabrachia canadensis to Polybrachia, making Crassibrachia sandersi Southward, 1968, and C. bra- a total of seven nominal species. siliensis Southward (1968). Scoring based on Ivanov (1963), Southward (1969). Scoring based on Southward (1968). The sper- Siboglinoides Ivanov, 1960 matophores are narrow and, though they are slightly Siboglinoides dibrachia Ivanov, 1960; two other nominal flattened, they are not given the leaf-like state. Rather species (see Ivanov, 1971; Southward, 1971b). they are similar to the spermatophores of Choanophorus, Scoring based on Ivanov (1963) and Southward (1971b). and Siphonobrachia, which seem to fall between the The posterior end is unknown. two states defined by Ivanov (1963). For the purposes Siboglinum Caullery, 1914 of this study all these taxa were considered as having Siboglinum weberi Caullery, 1914; 37 other nominal narrow spermatophores. species listed in Ivanov (1963). Southward (1961) re- Cyclobrachia Ivanov, 1960 solved the issue concerning the designation of the name Cyclobrachia auriculata Ivanov, 1960; only nominal spe- S. weberi, since Caullery (1914) had actually grouped cies. 16 different taxa under this name. Southward (1971b) Scoring based on Ivanov (1963). There are nine palps listed additional descriptions to bring the total to 51. and this is regarded as being ‘numerous’. Ivanov (1963: Subsequent descriptions (Flu¨ gel, 1990; Flu¨ gel & 366) wrote that the palps are free but closed at the base. Callsen-Cencic, 1993; Flu¨ gel & Langhof, 1983; Ivanov, Southward (1993:) states that the palps are closed and 1971; Southward, 1971a, 1972, 1975a) bring the total this is interpreted as meaning fused. The uncini of the of described nominal species to 65. Scoring is based girdle have teeth that all face in the same direction on Ivanov (1963) and Webb (1964d). Although some (Ivanov, 1963: fig. 145). The posterior end is unknown. members of Siboglinum have uncini with teeth all face Diplobrachia Ivanov, 1960 in the same direction, most have two groups of teeth Diplobrachia japonica Ivanov, 1960; five other nominal that oppose each other and this state is used in this species described (see Southward & Brattegard, 1968). study. Scoring based on Ivanov (1963) and Southward & Brat- Siphonobrachia Nielsen, 1965 tegard (1968). The number of palps varies within Di- Siphonobrachia ilyophora Nielsen, 1965 and S. lae- plobrachia with some taxa having three or four palps uensis Southward, 1991. and others having a pair. A pair of palps was coded as Scoring based on (Gupta & Little, 1969; Nielsen, 1965; present here but further study is required on this taxon. Southward, 1991). Although Nielsen (1965) suggests The posterior end is unknown. that S. ilyphora may have a zone of thickened papillae, it does not appear to be present in the relevant figures Galathealinum Kirkegaard, 1956 and was not found in S. lauensis Southward, 1991. The Galathealinum bruuni Kirkegaard, 1956; three other uncini of S. ilyphora all face in the same direction nominal species (see Adegoke, 1967). Webb (1971) sug- whereas those of S. lauensis oppose each other and the gested that two members of Galathealinum be removed state in the latter taxon is used in this study. The from this taxon and they were not considered in scoring spermatophore is known only for S. lauensis and was here. Scoring otherwise based on Ivanov (1963). The described as being narrow and compared with those of middle and posterior end is unknown. Oligobrachia by Southward (1991). The opisthosoma Heptabrachia Ivanov, 1952 was described for S. lauensis. Heptabrachia abyssicola Ivanov, 1952; six other species Spirobrachia Ivanov, 1952 in Ivanov (1963). However, Heptabrachia canadensis Spirobrachia grandis Ivanov, 1952; one other nominal Ivanov, 1962 was transferred by Southward (1969) to species (see Ivanov, 1963). Polybrachia. Scoring based on Ivanov (1963). The pos- Scoring based on Ivanov (1963). The posterior end is terior end is unknown. unknown. Lamellisabella Uschakov, 1933 Unibrachium Southward, 1972 Lamellisabella zachsi Uschakov, 1933; six other nominal Unibrachium colombianum Southward, 1972; one other species (see Southward, 1978b). nominal species (see Southward, 1978a). Scoring based on Ivanov (1963). The posterior end is Scoring based on Southward (1972, 1975a). Uni- unknown. brachium colombianum has a zone of thickened papillae Nereilinum Ivanov, 1961 and U. tenuifrenum Southward, 1975a seems to lack it. Nereilinum murmanicum Ivanov, 1961 and N. puncta- The condition in U. columbianum was used here. The tum Nielsen, 1965 posterior end is unknown. Scoring based on Ivanov (1963; 1975a). The presence of Zenkevitchiana Ivanov, 1957 pinnules on the palps and raised ventral glandular areas Zenkevitchiana longissima Ivanov, 1957; only nominal on the posterior trunk was based on N. murmanicum, species. though N. punctatum Nielsen, 1965 lacks them. Scoring based on Ivanov (1963). The spermatophores are Oligobrachia Ivanov, 1957 narrow but were compared with those of Spirobrachia by Oligobrachia doglei Ivanov, 1957; seven other nominal Ivanov (1963) i.e. leaf-shaped. For this study they are species (see Southward, 1978a]. scored as narrow. The posterior end is unknown. CLADISTICS OF SIBOGLINIDAE (POLYCHAETA) 79 10101011 10101011 ????1100 ????1100 10101011 . ’ ? ‘ ???????110? ?????11001011 ???1??11001101 ???1??11001101 ???1??11001011 ???1?? ???1??11001011 ???0??11001011 ?????1?? ???????? . Unknown is coded with ’ 1 ‘ ATRICES M APPENDIX 3 0001110000000000001?111010100111011011001011 0010000000000000001?111010101111011010101011 0001000000000000001?111010101111011010101101 0001110000000000001?1110101001 100110110110110101000100010100011101 0001???100000000001?1110100101 10011011010111010100010001010001110100011100 00011100000000000010110110101111011010101011 0010000000000000001?110110101111011010101011 0001110000000000001?1110100101???1??10101011 0001110000000000001011101010 10011?1111??0001010?0100010100011101 0001110000000000001?1110??10??? 1234567891011121314151617181920212223242526272829303132333435363738394041424344 100110110110101101000100010100011101????1100 10011011011000010100010001010001110100011100 000111010000000000101110100101?1001010101101 0100110000000000001?11011010 01001100000000000010111010101111011010101011 00100000000000000000000000000000000000000000 0001110100000000001?1110100101 0010110000000000001?1110101001 10011011110100001101010001010001110100011100 000111010000000000101110100101 0010000000000000001?0101010100011101000?1010 100110110101101011010100010100??? 0010110000000000001?1110100111 10011?1101??000101000100010100011101????1100 Zenkevitchiana Heptabrachia Lamellisabella Oligobrachia Nereilinum Polybrachia Siboglinoides Siphonobrachia Spirobrachia Siboglinum Unibrachium Cyclobrachia Crassibrachia Choanophorus Diplobrachia Galathealinum Arcovestia Escarpia Lamellibrachia Oasisia (A) Matrix of A/P coding scores used in both A/Pe and A/Pw analyses.Sabellariidae Present is codedAlaysia with Ridgeia Tevnia Riftia Sclerolinum Birsteinia 80 G. W. ROUSE

(B) Matrix of Multistate coding scores used in the multistate analysis. The OR separator ‘/’ is used for character 26 (Sperm packaging) for Sclerolinum since the presence of spermatophores could be excluded. Unknown is coded with ‘?’ and inapplicable with ‘–’.

123456789101112131415161718192021222324252627282930

Sabellariidae 00000–––––00000000000– 0000– 000 Alaysia 121111?0– 112?01?220210111??120 Arcovestia 121101?0– 112001?220210111??120 Escarpia 12110111101210132202????1??12? Lamellibrachia 12111110– 01210132202101112– 120 Oasisia 1211010101120013220210111??120 Tevnia 121101011112001?220210111??120 Ridgeia 121101110112001?2202101112– 120 Riftia 12110100– 11200132202101112– 120 Sclerolinum 0000– 0 ––––01?0112202101112– 110 Birsteinia 022000––––01?11211??????110111 Choanophorus 020000––––01?11211111120110121 Crassibrachia 0000– 0 ––––01?11211111120110111 Cyclobrachia 02?100––––01?1122101????011111 Diplobrachia 0020– 0 ––––01?1121101????111111 Galathealinum 022000––––01?1121????????11111 Heptabrachia 022000––––01?1121101????111111 Lamellisabella 022100––––0101122101????111121 Nereilinum 0000– 0 ––––01?11111111120110111 Oligobrachia 022000––––01011111111120110111 Polybrachia 022000––––01?11211011120111111 Siboglinoides 0020– 0 ––––01?1122111????110111 Siboglinum 012––0 ––––01011211111120110111 Siphonobrachia 022100––––01011221011?20010121 Spirobrachia 022100––––01?1122101????111121 Unibrachium 012––0 ––––01?11111??????110111 Zenkevitchiana 022000––––01?1122101????110111

APPENDIX 4 as the siboglinid, and all its descendants, to have a mid- trunk girdle, as seen in the holotype of Siboglinum NEW SYSTEMATICS weberi Caullery, 1914. The taxa of generic rank are not defined here since their monophyly was not investigated. Revised taxonomy of Siboglinidae (=Pogonophora and Vestimentifera) shown in indented format. Siboglinidae Siboglinidae is defined as the first polychaete, and all its descendants, Monilifera to have an gut occluded by expanded endoderm filled Sclerolinum with chemoautotrophic bacteria, as seen in the holotype Vestimentifera Alaysia, Arcovestia, Escarpia, Lamellibrachia, of Riftia pachyptila Jones, 1981a. Monilifera can be Oasisia, Ridgeia, Riftia, Tevnia defined based on apomorphy-based system such that it Frenulata is the first siboglinid, and all its descendants, to have Birstenia, Choanophorus, Crassibrachia, Cyclo- rings of chaetae (uncini) in the opisthosoma, as seen in brachia, Diplobrachia, Galathealinum, Hepta- the holotype of Sclerolinum magdalenae Southward, brachia, Lamellisabella, Nereilinum, Oligobrachia, 1972. Vestimentiferacan be defined as the first siboglinid Polybrachia, Siboglinum, Siboglinoides, Siphono- and all its descendants to have a vestimentum as seen brachia, Spirobrachia, Unibrachium, Zenke- in the holotype of Riftia pachyptia. Frenulata is defined vitchiana